Phylogenomic analysis of COVID-19 summer and winter outbreaks in Hong Kong: An observational study

Abstract

Background: Viral genomic surveillance is vital for understanding the transmission of COVID-19. In Hong Kong, breakthrough outbreaks have occurred in July (third wave) and November (fourth wave) 2020. We used whole viral genome analysis to study the characteristics of these waves.

Methods: We analyzed 509 SARS-CoV-2 genomes collected from Hong Kong patients between 22nd January and 29th November, 2020. Phylogenetic and phylodynamic analyses were performed, and were interpreted with epidemiological information.

Findings: During the third and fourth waves, diverse SARS-CoV-2 genomes were identified among imported infections. Conversely, local infections were dominated by a single lineage during each wave, with 96.6% (259/268) in the third wave and 100% (73/73) in the fourth wave belonging to B.1.1.63 and B.1.36.27 lineages, respectively. While B.1.1.63 lineage was imported 2 weeks before the beginning of the third wave, B.1.36.27 lineage has circulated in Hong Kong for 2 months prior to the fourth wave. During the fourth wave, 50.7% (37/73) of local infections in November was identical to the viral genome from an imported case in September. Within B.1.1.63 or B.1.36.27 lineage in our cohort, the most common non-synonymous mutations occurred at the helicase (nsp13) gene.

Interpretation: Although stringent measures have prevented most imported cases from spreading in Hong Kong, a single lineage with low-level local transmission in October and early November was responsible for the fourth wave. A superspreading event or lower temperature in November may have facilitated the spread of the B.1.36.27 lineage.

Keywords: COVID19; Next generation sequencing; Outbreak; Phylodynamic; Phylogenetic; SARS-CoV-2; Viral genome.

Fig. 1

Number of locally-acquired cases in Hong Kong between 22nd January and 29th November 2020. Data were adapted from the center for Health Protection .

Fig. 2

Whole genome phylogenetic analysis of 509 viral genomes showing the relationship between the genomes from locally-acquired and imported COVID-19 cases in Hong Kong from January to November 2020. The trees were constructed by maximum likelihood method with IQTree and Treetime. The reference genome Wuhan-Hu-1 (GenBank accession number MN908947.3) was used as the root of the tree. The substitution model GTR+F+I was used. (a) The entire phylogenetic tree. The blue branch indicates B.1.36.27 lineage from fourth wave. Pink, green and orange branches indicate B.1.1.63, B.1.1.141 and B.1.1.47 lineages from third wave, respectively. (b) A magnified figure focusing on the B.1.36.27 lineage. Blue triangles indicate Travelers C, D and E from Nepal, for whom the viral genomes are phylogenetically distinct to B.1.36.27 lineage. (c) GISAID and Nextstrain clade distribution of imported cases in Hong Kong. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Whole genome phylogenetic analysis of 509 viral genomes showing the relationship between the genomes from locally-acquired and imported COVID-19 cases in Hong Kong from January to November 2020. The trees were constructed by maximum likelihood method with IQTree and Treetime. The reference genome Wuhan-Hu-1 (GenBank accession number MN908947.3) was used as the root of the tree. The substitution model GTR+F+I was used. (a) The entire phylogenetic tree. The blue branch indicates B.1.36.27 lineage from fourth wave. Pink, green and orange branches indicate B.1.1.63, B.1.1.141 and B.1.1.47 lineages from third wave, respectively. (b) A magnified figure focusing on the B.1.36.27 lineage. Blue triangles indicate Travelers C, D and E from Nepal, for whom the viral genomes are phylogenetically distinct to B.1.36.27 lineage. (c) GISAID and Nextstrain clade distribution of imported cases in Hong Kong. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Whole genome phylogenetic analysis of 509 viral genomes showing the relationship between the genomes from locally-acquired and imported COVID-19 cases in Hong Kong from January to November 2020. The trees were constructed by maximum likelihood method with IQTree and Treetime. The reference genome Wuhan-Hu-1 (GenBank accession number MN908947.3) was used as the root of the tree. The substitution model GTR+F+I was used. (a) The entire phylogenetic tree. The blue branch indicates B.1.36.27 lineage from fourth wave. Pink, green and orange branches indicate B.1.1.63, B.1.1.141 and B.1.1.47 lineages from third wave, respectively. (b) A magnified figure focusing on the B.1.36.27 lineage. Blue triangles indicate Travelers C, D and E from Nepal, for whom the viral genomes are phylogenetically distinct to B.1.36.27 lineage. (c) GISAID and Nextstrain clade distribution of imported cases in Hong Kong. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

(a) Time-resolved phylogenetic tree of 499 viral genomes from December 2019 to November 2020. The scale bars indicate the substitution rates per site per year. (b) Evolutionary rate estimate using root-to-tip (RtT) regression analysis for B.1.1.63 lineage in third wave.

Fig. 4

Single nucleotide mutations within B.1.1.63 in third wave and B.1.36.27 in fourth wave. The most common non-synonymous mutation are highlighted in yellow. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)