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Extensive Mammalian Ancestry of Pandemic (H1N1) 2009 Virus
EID Journal Home > Volume 16, Number 2–February 2010
Volume 16, Number 2–February 2010 Dispatch Extensive Mammalian Ancestry of Pandemic (H1N1) 2009 Virus Natalia A. Ilyushina,1 Jeong-Ki Kim,1 Nicholas J. Negovetich,1 Young-Ki Choi,1 Victoria Lang, Nicolai V. Bovin, Heather L. Forrest, Min-Suk Song, Philippe Noriel Q. Pascua, Chul-Joong Kim, Robert G. Webster, and Richard J. Webby Author affiliations: St. Jude Children's Research Hospital, Memphis, Tennessee, USA (N.A. Ilyushina, J.-K. Kim, N.J. Negovetich, V. Lang, H.L. Forrest, R.G. Webster, R.J. Webby); D.I. Ivanovsky Institute of Virology, Moscow, Russia (N.A. Ilyushina); Korea Research Institute of Bioscience and Biotechnology, Daejeon, Republic of Korea (J.-K. Kim); Chungbuk National University College of Medicine and Medical Research Institute, Cheongju, Republic of Korea (Y.-K. Choi, M-S Song, P.N.Q. Pascua); Shemyakin Institute of Bioorganic Chemistry, Moscow (N.V. Bovin); Chungnam National University College of Veterinary Medicine, Daejeon (C.-J. Kim); and University of Tennessee Health Science Center, Memphis (R.G. Webster, R.J. Webby)
Suggested citation for this article
Abstract We demonstrate that the novel pandemic influenza (H1N1) viruses have human virus–like receptor specificity and can no longer replicate in aquatic waterfowl, their historic natural reservoir. The biological properties of these viruses are consistent with those of their phylogenetic progenitors, indicating longstanding adaptation to mammals.
Pandemic (H1N1) 2009 virus strains were recently reported to be reassortants of the North American and European swine lineages (6). Phylogenetic evidence suggests that this reassortment event occurred 10–17 years ago (7). These data suggest that the current pandemic (H1N1) 2009 virus strains should have receptor specificity typically found in the HA of mammalian viruses (Neu5Acα2,6Gal). In addition, they may have lost the ability to replicate in avian hosts, the natural reservoir species. To test these hypotheses, we examined the biological properties of pandemic (H1N1) 2009 virus, including receptor specificity, erythrocyte binding, and ability to replicate in avian species.
The Study We first tested species-specific erythrocyte agglutination by the pandemic (H1N1) 2009 isolates A/California/04/2009 and A/Tennessee/1-560/2009 and by other isolates from humans, swine, and birds (Table 1). The pandemic (H1N1) 2009 isolates showed reduced or absent agglutination of goose and chicken erythrocytes. Human and swine H1N1 viruses were agglutinated by turkey, guinea pig, chicken, and goose erythrocytes, and all erythrocytes we tested except those of swine were agglutinated by avian isolates (Table 1).
We next measured the receptor binding of the 2 pandemic (H1N1) 2009 isolates to sialic substrates, both natural (fetuin) and synthetic (3´-sialyllactose [3´SL] and 6´-sialyllactosamine [6´SLN] attached to a polyacrylic carrier) (Figure). The binding pattern to fetuin was identical among all isolates tested (association constant Kass ≈ 5.8 ± 0.5, 1/μM sialic acid). The currently circulating human and pandemic influenza (H1N1) viruses showed a preference for 6´SLN and negligible binding to the avian-type 3´SL. A similar pattern was observed for 2 recent swine viruses, which bound only to 6´SLN receptors with nearly equal affinity as pandemic (H1N1) 2009 isolates. As expected, the 2 avian H1 viruses bound strongly only to 3´SL (Figure).
To assess the infectivity and pathogenicity of pandemic (H1N1) 2009 virus strain A/California/04/2009 in terrestrial (chickens, quails) and aquatic (domestic and wild ducks) avian species, we inoculated 10 birds of each species by intranasal, intraocular, and intratracheal instillation with ≈106.0 of the 50% egg infectious dose (EID50) of the virus. We then observed the birds for the next 2 weeks for death and for viral shedding and signs of illness. No birds showed obvious clinical signs of disease. Virus was detected only on postinoculation day 1 in infected chickens and ducks and only in tracheal samples at low titers (<1.7 log10 of the EID50/mL ) (Table 2). However, no later shedding of virus was observed, indicating that the virus detected on postinoculation day 1 could have been caused by residual virus particles after inoculation. In contrast, our results revealed that the A/California/04/2009 strain efficiently infected quails with significantly higher titers (<3.4 log10 EID50/mL until postinoculation day 5; p<0.05) in both oropharyngeal and cloacal swab specimens (Table 2). The virus was detected in the trachea (1.7 log10 EID50/g), lungs (2.3 log10 EID50/g), and cecal tonsil (0.8 log10 EID50/g) of quails on postinoculation day 5.
The potential bird-to-bird intraspecies transmission of the A/California/04/2009 pandemic (H1N1) 2009 virus strain in avian species was also examined by introducing 3 contact birds to the inoculated birds' cages on postinoculation day 1. There was no subsequent evidence of viral shedding through the upper respiratory tract or fecal-oral route in any group of birds except 1 of 3 contact quails (Table 2). Oropharyngeal virus titers in this quail were l.7 and 1.5 log10 EID50/mL on postinoculation days 3 and 5, indicating that productive viral replication was occurring.
Suggested Citation for this Article Ilyushina NA, Kim J-K, Negovetich NJ, Choi Y-K, Lang V, Bovin NV, et al. Extensive mammalian ancestry of pandemic (H1N1) 2009 virus. Emerg Infect Dis [serial on the Internet]. 2010 Feb [date cited]. http://www.cdc.gov/EID/content/16/2/314.htm
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