Origin and fate of A/H1N1 influenza in Scotland during 2009

Abstract

The spread of influenza has usually been described by a ‘density’ model, where the largest centres of population drive the epidemic within a country. An alternative model emphasizing the role of air travel has recently been developed. We have examined the relative importance of the two in the context of the 2009 H1N1 influenza epidemic in Scotland. We obtained genome sequences of 70 strains representative of the geographical and temporal distribution of H1N1 influenza during the summer and winter phases of the pandemic in 2009. We analysed these strains, together with another 128 from the rest of the UK and 292 globally distributed strains, using maximum-likelihood phylogenetic and Bayesian phylogeographical methods. This revealed strikingly different epidemic patterns within Scotland in the early and late parts of 2009. The summer epidemic in Scotland was characterized by multiple independent introductions from both international and other UK sources, followed by major local expansion of a single clade that probably originated in Birmingham. The winter phase, in contrast, was more diverse genetically, with several clades of similar size in different locations, some of which had no particularly close phylogenetic affinity to strains sampled from either Scotland or England. Overall there was evidence to support both models, with significant links demonstrated between North American sequences and those from England, and between England and East Asia, indicating that major air-travel routes played an important role in the pattern of spread of the pandemic, both within the UK and globally.

Contrasting the epidemiological and evolutionary dynamics of influenza spatial transmission

“…A slightly different phylogeographic pattern was observed in Scotland, where the spring 2009 pandemic wave was characterized by the expansion of a major clade originating from Birmingham, England, together with multiple introductions from both international and other UK sources [34]. By contrast, the autumn pandemic wave in Scotland was more genetically diverse with several co-dominant clades in individual locations, indicative of widespread gene flow [34]. The examples of the USA and Scotland during the 2009 A/H1N1 pandemic suggest that spatial patterns may vary substantially between temperate locations.…”

“…However, such spatial structure was broken down by extensive global mixing during the autumn pandemic wave, which was dominated by a single clade that was prevalent in spring in New York City [33]. A slightly different phylogeographic pattern was observed in Scotland, where the spring 2009 pandemic wave was characterized by the expansion of a major clade originating from Birmingham, England, together with multiple introductions from both international and other UK sources [34]. By contrast, the autumn pandemic wave in Scotland was more genetically diverse with several co-dominant clades in individual locations, indicative of widespread gene flow [34].…”

“…extensive mixing [34] rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120199 information on air travel volumes with local work commute patterns, together with population demographics and seasonality factors. Such large-scale modelling efforts predicted that an early peak of pandemic influenza A/H1N1 virus activity would occur in October/November 2009 in the Northern Hemisphere, several weeks before vaccination campaigns could be carried out, and that antiviral use could delay peak pandemic timing.…”

Inferring influenza global transmission networks without complete phylogenetic information

“…1), which are known to be seeding a new epidemic in each hemisphere with a 6-month shift (Nelson and Holmes 2007). As no H1 sequences were documented in South America prior to the H1N1/09 pandemic ( Figure S7), the biphasic H1 diversity in this region is likely a reflection of the biphasic pandemic that occurred in 2009, which is rem-iniscent of the biphasic pandemic diversity observed in the USA or in Scotland (Lycett et al 2012).…”

Lessons from Ebola: Improving infectious disease surveillance to inform outbreak management

“…However, exponential growth during the early stages of an outbreak is not expected in all circumstances (33), such as when R 0 ≈1, a realistic scenario for which large outbreaks (hundreds of cases or more) is entirely possible (34) or when there are multiple introductions separated in time and space, some of which die out due simply to demographic stochasticity. This was the case with pandemic H1N1 influenza A in Scotland in 2009, as indicated by the analysis of virus sequence data (35). The history of ebolavirus in Liberia in 2014 may also have involved multiple introductions (32) but, again, this can only be confirmed from virus genome sequence data.…”