Persistence of H5 and H7 Avian Influenza Viruses in Water

Brown, Justin D.; Swayne, David E.; Cooper, Robert J.; Burns, Rachel E.; Stallknecht, David E.

doi:10.1637/7636-042806r.1

Cited by 290 publications

(273 citation statements)

References 15 publications

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“…In aquatic birds, the main route of transmission is thought to be faecal-oral [2]. While the proximity of many birds in large flocks can lead to rapid transmission and large-scale outbreaks, it has recently been appreciated that prolonged persistence of influenza virus in the aquatic environment is possible [10][11][12][13]. This might lead to additional, indirect chains of transmission [14][15][16][17][18].…”

Section: Introductionmentioning

confidence: 99%

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

et al. 2014

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Trade-offs between different components of a pathogen's replication and transmission cycle are thought to be common. A number of studies have identified trade-offs that emerge across scales, reflecting the tension between strategies that optimize within-host proliferation and large-scale population spread. Most of these studies are theoretical in nature, with direct experimental tests of such cross-scale trade-offs still rare. Here, we report an analysis of avian influenza A viruses across scales, focusing on the phenotype of temperaturedependent viral persistence. Taking advantage of a unique dataset that reports both environmental virus decay rates and strain-specific viral kinetics from duck challenge experiments, we show that the temperature-dependent environmental decay rate of a strain does not impact within-host virus load. Hence, for this phenotype, the scales of within-host infection dynamics and between-host environmental persistence do not seem to interact: viral fitness may be optimized on each scale without cross-scale trade-offs. Instead, we confirm the existence of a temperature-dependent persistence trade-off on a single scale, with some strains favouring environmental persistence in water at low temperatures while others reduce sensitivity to increasing temperatures. We show that this temperature-dependent trade-off is a robust phenomenon and does not depend on the details of data analysis. Our findings suggest that viruses might employ different environmental persistence strategies, which facilitates the coexistence of diverse strains in ecological niches. We conclude that a better understanding of the transmission and evolutionary dynamics of influenza A viruses probably requires empirical information regarding both within-host dynamics and environmental traits, integrated within a combined ecological and within-host framework.

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Section: Introductionmentioning

confidence: 99%

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

et al. 2014

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“…Each virus and water sample combination was maintained at 10, 17, and 28°C, respectively, with low-temperature incubators and water baths. The three incubation temperatures were selected because they are temperatures that have been used extensively in studies described in the literature and they represent water temperatures that would be encountered in aquatic habitats of waterfowl (6,15,16,19). In addition, 15 ml of each water sample with no infective AAF was maintained at each temperature.…”

Section: Methodsmentioning

confidence: 99%

“…The temperature, pH, and salinity of the water have been identified as important determinants of the duration of persistence (8,(15)(16)(17)(18)(19). Using modified distilled water as a laboratory model, Brown et al (16) determined that AI viruses are most stable in water with a neutral-to-basic pH (7.4 to 8.2), low salinity (Ͻ20 ppt), and a low temperature (Ͻ17°C).…”

mentioning

confidence: 99%

Abiotic Factors Affecting the Persistence of Avian Influenza Virus in Surface Waters of Waterfowl Habitats

Keeler

Dalton

Cressler

et al. 2014

Appl Environ Microbiol

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dAvian influenza (AI) virus can remain infectious in water for months, and virus-contaminated surface water is considered to be a source of infection within wild waterfowl populations. Previous work has characterized the effects of pH, salinity, and temperature on viral persistence in water, but most of that work was done with modified distilled water. The objective of this study was to identify the abiotic factors that influence the duration of AI virus persistence in natural surface water. Surface water samples were collected from 38 waterfowl habitats distributed across the United States. Samples were submitted to the U.S. Geological Survey National Water Quality Laboratory for chemical analysis and the University of Georgia for viral reduction time analysis. Samples were filtered with 0.22-m filters, and the durations of persistence of three wild-bird-derived influenza A viruses within each water sample at 10, 17, and 28°C were determined. The effects of the surface water physicochemical factors on the duration of AI viral persistence in laboratory experiments were evaluated by multivariable linear regression with robust standard errors. The duration of AI virus persistence was determined to be longest in filtered surface water with a low temperature (<17°C), a neutral-to-basic pH (7.0 to 8.5), low salinity (<0.5 ppt), and a low ammonia concentration (<0.5 mg/liter). Our results also highlighted potential strain-related variation in the stability of AI virus in surface water. These results bring us closer to being able to predict the duration of AI virus persistence in surface water of waterfowl habitats. Wild birds are considered to be the primordial reservoir for influenza A virus, with species within the orders Anseriformes and Charadriiformes having the largest and most diverse genetic pool of viruses (1, 2). Within these wild bird hosts, replication of avian influenza (AI) virus occurs primarily in the epithelial cells of the intestinal tract, and large amounts of virus are shed in feces (3, 4). The virus contaminates the surrounding aquatic environment, where it remains infectious, facilitating indirect transmission between birds (5-8). Environmental persistence of AI virus has been determined to be important for the epidemiology of the virus within wild bird populations and within aquatic habitats, and surface water is considered to be the major site of environmental contamination (9-12).The persistence of AI virus in water has been confirmed through environmental surveillance and laboratory-based investigations (6, 13-16). The temperature, pH, and salinity of the water have been identified as important determinants of the duration of persistence (8,(15)(16)(17)(18)(19). Using modified distilled water as a laboratory model, Brown et al. (16) determined that AI viruses are most stable in water with a neutral-to-basic pH (7.4 to 8.2), low salinity (Ͻ20 ppt), and a low temperature (Ͻ17°C). These general trends are supported by further laboratory investigations using natural surface water samples (8,15,1...

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“…For effective viral replication, influenza viruses require a certain level of stability toward inactivating factors, such as acidic pH, heat, and chemical denaturants that promote the conformational change of HA into its fusogenic form, leading to viral inactivation (40,48). An optimal range for the pH of HA activation is required that is low enough to avoid inactivation in the environment or in mildly acidic tissues (35,77) but high enough to allow membrane fusion to occur before the virus is trafficked to the lysosome (35,78). Influenza virus mutations that increase the pH of HA activation increase the susceptibility of the virus to acid inactivation (31).…”

Section: Figmentioning

confidence: 99%

The Matrix Gene Segment Destabilizes the Acid and Thermal Stability of the Hemagglutinin of Pandemic Live Attenuated Influenza Virus Vaccines

O’Donnell

Vogel

Matsuoka

et al. 2014

J Virol

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The threat of future influenza pandemics and their potential for rapid spread, morbidity, and mortality has led to the development of pandemic vaccines. We generated seven reassortant pandemic live attenuated influenza vaccines (pLAIVs) with the hemagglutinin (HA) and neuraminidase (NA) genes derived from animal influenza viruses on the backbone of the six internal protein gene segments of the temperature sensitive, cold-adapted (ca) A/Ann Arbor/60 (H2N2) virus (AA/60 ca) of the licensed seasonal LAIV. The pLAIV viruses were moderately to highly restricted in replication in seronegative adults; we sought to determine the biological basis for this restriction. Avian influenza viruses generally replicate at higher temperatures than human influenza viruses and, although they shared the same backbone, the pLAIV viruses had a lower shutoff temperature than seasonal LAIV viruses, suggesting that the HA and NA influence the degree of temperature sensitivity. The pH of HA activation of highly pathogenic avian influenza viruses was greater than human and low-pathogenicity avian influenza viruses, as reported by others. However, pLAIV viruses had a consistently higher pH of HA activation and reduced HA thermostability compared to the corresponding wild-type parental viruses. From studies with single-gene reassortant viruses bearing one gene segment from the AA/60 ca virus in recombinant H5N1 or pH1N1 viruses, we found that the lower HA thermal stability and increased pH of HA activation were associated with the AA/60 M gene. Together, the impaired HA acid and thermal stability and temperature sensitivity likely contributed to the restricted replication of the pLAIV viruses we observed in seronegative adults. IMPORTANCEThere is increasing evidence that the HA stability of influenza viruses depends on the virus strain and host species and that HA stability can influence replication, virulence, and transmission of influenza A viruses in different species. We investigated the HA stability of pandemic live attenuated influenza vaccine (pLAIV) viruses and observed that the pLAIV viruses consistently had a less stable HA than the corresponding wild-type influenza viruses. The reduced HA stability and temperature sensitivity of the pLAIV viruses may account for their restricted replication in clinical trials.

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Persistence of H5 and H7 Avian Influenza Viruses in Water

Cited by 290 publications

References 15 publications

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Abiotic Factors Affecting the Persistence of Avian Influenza Virus in Surface Waters of Waterfowl Habitats

The Matrix Gene Segment Destabilizes the Acid and Thermal Stability of the Hemagglutinin of Pandemic Live Attenuated Influenza Virus Vaccines

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