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THE EMERGENCE OF PANDEMIC INFLUENZA A
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Age distribution of deaths of females from influenza in 1918 and in the first quarter of 1919 200
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2nd Quarter of 1918 3rd Quarter of 1918 4th Quarter of 1918 1st Quarter of 1919 150
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Proportion per 100 deaths of all ages
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0 10 15 15 20 20 25 25 30 30 35 35 40 40 45 45 50 50 55 55 60 60 65 65 70 70 75 75 80 80 85 5 10 85 & up 0 5
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Age group (yr)
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FIGURE 13.12 Skewed mortality in the 1918 pandemic, which included, unexpectedly, younger persons.
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CRYSTAL STRUCTURE OF THE 1918 INFLUENZA HA
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TABLE 13.8 In vivo Properties of Recombinant In uenza Viruses Containing Genes of the 1918 In uenza Virus Virusa Parental WSN virus 1918 HA/NA 1918 HA/NA/M 1918 HA/NA/M/ NS 1918 HA/NA/M/NS/NP
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Titerb-(plaque-forming units/mL) % Weight Lossc 2.2 107 2.1 107 1.4 108 2.1 107 1.4 108 28.4 20.9 28.8 23.7 24.5
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Lung Titersd 6.7 0.2 7.3 0.1 7.9 0.2 7.3 0.2 7.4 0.2
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LD50e 2.5 2.75 2.75 3.25 1.75
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All viral genomic segments were derived from the A/WSN/33 virus unless otherwise indicated. Titer of virus stocks prepared on MDCK cells. c Mean percentage weight loss on day 4 p.i. ( ve mice per group). d Mean lung titers of four mice on day 4 p.i. expressed as ElD50/mL SE. e Expressed as the log10 plaque-forming units required to give 1 LD50. Source: Adapted from Reference 93.
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abundant protein in the viral particle, lines the inner layer of the viral lipid envelope, and is involved in regulating nuclear export of viral RNPs. The M1 protein controls transport of RNPs into the nucleus during infection of the cell and restricts reentry of RNAs into the nucleus at the later stages of infection.89 M1 may also inhibit viral transcription at a late stage of infection and regulate the switch from replication to virus assembly.90 An analysis of the M gene from 1918 in uenza91 has not to date identi ed any amino acid change suggestive of enhanced virulence. Indeed, the 1918 M gene does not code for any of the single amino acid changes that correlate with virulence in previous experimental studies of other in uenza A viruses of a high growth phenotype. More recently, it has been appreciated that balanced HA NA interactions are crucial for the most ef cient replication of in uenza, so certain combinations of HA and NA may have to be optimal for virulence.92 However, biological studies of the HA and NA genes of 1918 in uenza failed to demonstrate transfer of intrinsic enhanced virulence in mice93 (Table 13.8).
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13.16 CRYSTAL STRUCTURE OF THE 1918 INFLUENZA HA: THE KEY TO UNDERSTANDING INFLUENZA VIRUS VIRULENCE Unexpectedly, the nucleotide sequence of the 1918 virus HA gene94 failed to show an expected hydrophobic cleavage sequence at the HA1 HA2 junction, or crucial glycosylation patterns and particular receptor binding motifs, which are known virulence factors with some in uenza A viruses. Our most recent studies91 detected nucleotide changes at the receptor binding site sequences extracted from London and U.S. lung samples from 1918 in uenza victims, which hinted at the possibility of more than one virus circulating, perhaps with varying biological properties. Receptor binding site substitutions in the HA are known to confer antigenic
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THE EMERGENCE OF PANDEMIC INFLUENZA A
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changes in the important epitope B of the HA58: one could speculate that more than one antigenic HA was circulating. Biological analysis of the 1918 HA expressed in vaccinia virus also indicated a 1918 virus with curious receptor binding properties able to agglutinate HAs of chicken, guinea pig, and human origin (A. Elliot, R. Daniels, and J. S. Oxford, in preparation). Thus, our new data indicates that the receptor site on the 1918 HA appeared to have the ability to bind both to 2,3 and 2,6 receptors on sialylated glycoproteins; human and avian in uenza viruses are known to bind to 2,6 and 2,3 linkages, respectively. The crystal structure of the uncleaved human H1 HA (HA0) from 1918 in uenza virus has been reported by Stevens et al.95 and Gamblin et al.96 The 1918 virus A/South Carolina/1/18 was cloned and expressed in a baculovirus expression system. The HA0 was crystallized at pH5.5 and its structure determined by molecular replacement to 3.0 A resolution. The overall structure was similar in many respects to the in uenza A H3 HA reported previously.97 Superimposition of the 1918 HA2 (H1 subtype) domains with other time-related HAs indicated that the 1918 HA most closely resembles the avian H5 subtype at the receptor. On the other hand, the cleavage site loop of the 1918 HA0 is relatively unique compared to H3 and H5 HAs. There may be an in uence of nearby glycosylation sites. Unexpectedly, the 1918 HA0 was not cleaved with trypase from human lung, whereas trypsin cleaved the HA molecule. However, most interest is focused on the receptor binding site, which is situated in a shallow pocket in the HA1 distal domain near the HA tip. As mentioned earlier, in general, avian viruses preferentially bind to receptors that have an a-2,3 linkage, whereas human-adapted viruses prefer the a-2,6 linkage. Unexpectedly, in the 1918 HA the avian type residues Gln226 and Gly220 predominate at and around the receptor binding site. Morphologically, the receptor binding site of the 1918 HA is more like that of avian HAs than human HAs. Thus the pocket of 1918 HA is narrower than the corresponding region of the human H3 HA. Overall these features could result in unique cleavage and/or fusion properties as well as receptor binding speci cities of the 1918 HA. In a parallel study, Gamblin et al.96 concentrated particularly on the receptor binding properties of the 1918 HA as compared to 1934 H1, 1930 swine H1 and avian H1 viruses. Two of the ve HAs reported from 1918 have receptor binding sites indistinguishable from 1930 swine HA. The other three 1918 HAs differ at residue 225.91 Irrespective of the amino acid difference at residue 225, all the sequenced 1918 HAs recognize human receptors and, therefore, they would all be able to infect human cells and presumably spread from human to human.
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13.17 COULD A MIXTURE OF PNEUMOCOCCUS AND DRUG-RESISTANT INFLUENZA A VIRUS BE THE BASIS OF A HYPERVIRULENT INFECTION During the Edwardian years at the beginning of the twentieth century, pneumonia was a leading cause of death worldwide. Most of these pneumonias were caused by
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