Genomic epidemiology of SARS-CoV-2 in Russia reveals recurring cross-border transmission throughout 2020

Abstract

In 2020, SARS-CoV-2 has spread rapidly across the globe, with most nations failing to prevent or substantially delay its introduction. While many countries have imposed some limitations on trans-border passenger traffic, the effect of these measures on the global spread of COVID-19 strains remains unclear. Here, we report an analysis of 3206 whole-genome sequences of SARS-CoV-2 samples from 78 regions of Russia covering the period before the spread of variants of concern (between March and November 2020). We describe recurring imports of multiple COVID-19 strains into Russia throughout this period, giving rise to 457 uniquely Russian transmission lineages, as well as repeated cross-border transmissions of local circulating variants out of Russia. While the phylogenetically inferred rate of cross-border transmissions was somewhat reduced during the period of the most stringent border closure, it still remained high, with multiple inferred imports that each led to detectable spread within the country. These results indicate that partial border closure has had little effect on trans-border transmission of variants, which helps explain the rapid global spread of newly arising SARS-CoV-2 variants throughout the pandemic.

Fig 1

Dynamics of Pango lineages frequencies in Russia (top row) and in the rest of the world (bottom row) before November 2020. Sequences are ordered by sampling date, split into 14 day bins. Color legend as in Fig 1.

Fig 2

Phylogenetic categorization of sequences into Russian transmission lineages, stem clusters, stem-derived singletons (a) and singletons (b), and inference of IBTs (c) and OBTs (d). I, node ancestral to an IBT event; O, node ancestral to an OBT event.

Fig 3. Russian transmission lineages.

In the top part of the figure, each horizontal line represents a Russian transmission lineage, ordered by the date of the earliest sample. For Russian transmission lineages descended from a Russian stem cluster, the small gray circle in the left identifies the earliest Russian sequence date for the corresponding stem cluster. The three bottom lines represent Russian singletons, Russian stem-derived singletons, and Russian stem clusters (see S2 Fig for terminology for lineage notation). Circles represent samples taken on a particular date, with circle size representing the number of samples. Circle color indicates the PANGOLIN designation of the corresponding sample. Gray lines without colored terminal nodes are transmission lineages without dated sequences.

Fig 4. Timeline for inbound and outbound transmissions of SARS-CoV-2 variants.

Bars correspond to individual IBTs (red) and OBTs (orange), with the left end of the bar corresponding to the date estimated for the corresponding node by the “node.dating” procedure [13] from the “ape” package of R language [14], and the right end of the bar corresponding to the date of the earliest Russian (for IBTs) or non-Russian (for OBTs) sample among the node’s descendants. Line width identifies the number of sequences descendant to the IBT or OBT. Only cases with available sample dates are shown. Yellow background indicates the period of the most stringent closure of Russia’s borders. Also shown is the number of international travellers going through Russian airports and the total number of Russian samples obtained in the corresponding month.

Fig 5. IBTs and OBTs in the history of the B.1.1.238 lineage.

Branch lengths are measured in the number of changes. The number at the end of the sequence id represents the number of identical sequences (including the one shown) identified in the region on this date. Samples from Russia are identified with red labels. OBTs are indicated by a purple star and “O” letter.