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Phylodynamics Reveals the Role of Human Travel and Contact Tracing in Controlling COVID-19 in Four Island Nations

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Phylodynamics Reveals the Role of Human Travel and Contact Tracing in Controlling COVID-19 in Four Island Nations medRxiv preprint doi: https://doi.org/10.1101/2020.08.04.20168518; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license . Phylodynamics reveals the role of human travel and contact tracing in controlling COVID-19 in four island nations 1,2,†, 1,2,3,†, 1,2 Jordan Douglas ∗, Fábio K. Mendes ∗, Remco Bouckaert , Dong Xie1,2, Cinthy L. Jiménez-Silva1,3, Christiaan Swanepoel1,2, Joep de Ligt4, Xiaoyun Ren4, Matt Storey4, James Hadfield5, Colin R. Simpson6, Jemma L. Geoghegan4,7, David Welch1,2 and Alexei J. Drummond1,2,3 1Centre for Computational Evolution, The University of Auckland, Auckland, New Zealand 2School of Computer Science, The University of Auckland, Auckland, New Zealand 3School of Biological Sciences, The University of Auckland, Auckland, New Zealand 4Institute of Environmental Science and Research, Wellington, New Zealand. 5Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA 6School of Health, Victoria University of Wellington, Wellington, New Zealand 7Department of Microbiology and Immunology, University of Otago, Dunedin, New Zealand †To whom correspondence should be addressed; Email: [email protected], [email protected]. ∗Authors contributed equally to this work. MAIN TEXT The work below has not been peer reviewed Abstract Most populated corners of the planet have been exposed to SARS-CoV-2, the coronavirus behind the COVID-19 pandemic. We examined the progression of COVID-19 in four island nations that fared well over the first three months of the pandemic: New Zealand, Australia, Iceland, and Taiwan. Using Bayesian phylodynamic methods, we estimated the effective reproduction number of COVID-19 in the four islands as 1–1.4 during early stages of the pandemic, and show that it declined below 1 as human movement was restricted. Our reconstruction of COVID-19’s phylogenetic history indicated that this disease was introduced many times into each island, and that introductions slowed down markedly when the borders closed. Finally, we found that New Zealand clusters identified via standard health surveillance largely agreed with those defined by genomic data. Our findings can assist public health decisions in countries with circulating SARS-CoV-2, and support efforts to mitigate any second waves or future epidemics. 1 NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice. medRxiv preprint doi: https://doi.org/10.1101/2020.08.04.20168518; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license . Douglas et al. July 2020 • Introduction Many continued hoping that the epidemic would soon die out and they and their families be spared. Thus they felt under no obligation to make any change in their habits, as yet. Plague was an unwelcome visitant, bound to take its leave one day as unexpectedly as it had come. Albert Camus (“The Plague”, 1947) The respiratory tract illness caused by Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) known as Coronavirus Disease 2019 (COVID-19; Rothan and Byrareddy, 2020) has caused substantial global health and economic impact, and the global epidemic appears far from over. COVID-19 was first detected in the city of Wuhan, Hubei province (China) in late 2019; (Zhu et al., 2020). By 11 March 2020 there were 100,000 cases across 114 countries leading to the World Health Organization (WHO) declaring a pandemic (World Health Organization, 2020b). By the end of April, 3 million cases and 200,000 deaths had been confirmed (World Health Organization, 2020a), with over half of the world population under stay-at-home orders (Sandford, 2020). COVID-19 has now been characterised extensively. The average number of people each case goes on to infect (known as the effective reproduction number, Re), for example, has been estimated as 1–6 during the early stages of the outbreak (Liu et al., 2020; Binny et al., 2020; Alimohamadi et al., 2020). Because COVID-19 often causes mild symptoms (Day, 2020b,a), the difference between the true and reported number of cases could be of an order of magnitude (Li et al., 2020a; Lu et al., 2020). Fortunately, Re has since declined in many locations to less than 1 as result of social distancing, travel restrictions, contact tracing, among other mitigation efforts (Binny et al., 2020; Chinazzi et al., 2020). At the moment of writing, different parts of the world tell contrasting stories about their struggle against COVID-19. New Zealand, Iceland, and Taiwan, for example, have fared comparatively well with smaller infection peaks and lower excess mortalities compared to many mainland countries (World Health Organization, 2020a; FT Visual & Data Journalism team, 2020). Australia was close to elimination, but in late June a second uncontrolled outbreak began in the state of Victoria. Nevertheless the initial experience of these four countries was similar. They all responded to COVID-19 by closing their borders and requiring isolation or quarantine of those who were allowed through (Hale et al., 2020), and either restricting or discouraging human movement (Apple, 2020). These countries provide excellent case studies to characterise the effects of human travel on epidemic spread, a critical endeavor when facing the threat of a COVID-19 second wave and global endemicity. Mathematical methods for studying epidemics are as diverse as the diseases they target, making varied 2 medRxiv preprint doi: https://doi.org/10.1101/2020.08.04.20168518; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license . Douglas et al. July 2020 • use of surveillance and genetic data, and ranging from models of mathematical epidemiology (Grassly and Fraser, 2008; Binny et al., 2020; Ferretti et al., 2020; Hethcote, 2000) to phylodynamic models (Volz et al., 2013). The latter enjoy the comparable timescales of epidemiological and evolutionary processes, which result from short viral generation times and high viral mutation rates (20–40 mutations per year for SARS-CoV-2; Lai et al., 2020; Li et al., 2020b; Rambaut, 2020). By modelling the transmission process as phylogenetic trees (Fig. 1), phylodynamic and molecular evolution models can be coupled to reconstruct the mutational history of viral genomes (Li et al., 2020b; Rambaut, 2020; Lai et al., 2020), elucidating the epidemiological processes that shaped them. We have sequenced 217 SARS-CoV-2 genomes from New Zealand, and evaluated the effects of travel and movement restrictions on disease progression in New Zealand, Australia, Iceland, and Taiwan. Finally, we examined the spatiotemporal structure of New Zealand’s COVID-19 epidemic, by comparing genetically identified clusters to those independently identified by public health surveillance. Phylodynamic models In the study of disease phylodynamics, a complete epidemic can be modelled as a rooted, binary phylo- genetic trees whose N tips are all infected individuals (Fig. 1), and whose characteristics and drivers we wish to uncover. In a rapidly growing epidemic the age of this tree is a good proxy for the duration of the infection in the population. Because it is seldom possible to sample the entire infected population, one instead reconstructs a subtree from a sample of cases of size n, where n < N. This sample provides n T viral genomic sequences we refer to as D, as well as each sequence’s sampling date, collectively represented by vector y. D and y thus constitute the input data, and are herein referred to as the “samples”. In the case of structured phylodynamic models, samples in y are further annotated by “deme” – a geographical unit such as a city, a country, or a continent. A Bayesian phylodynamic model is characterised by the following unnormalised posterior probability density function: f ( , m , q , q D, y) ∝ P(D , m , q ) f ( q ) f (m , q , q ), (1) T c s tj jT c s T j t pr c s t where P(D , m , q ) is the phylogenetic likelihood of tree given alignment D, whose sequences accu- jT c s T mulate substitutions at rate m under a substitution model with parameters q . f ( q ) is the probability c s T j t density function of the tree prior sampling distribution, given tree prior parameters qt (in this study we 3 medRxiv preprint doi: https://doi.org/10.1101/2020.08.04.20168518; this version posted August 6, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license . Douglas et al. July 2020 • consider a range of phylodynamic models that differ in their tree prior; see below and Supplementary materials). Finally, fpr(mc, qs, qt) is the prior distribution on the remaining parameters. Full infection tree Sampled infection tree a) t0 b) Interval 1 Sampled ψ1 r1 =1 µ1 λ1 Infected Removed R m m t 1,2 2,1 1 Interval 2 µ2 λ S S 2 Infected Removed ψ2 r2 =1 tf S S S R S Sampled I Time Fig. 1: Depiction of the MTBD model.
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