Spatiotemporal Evolution of SARS-CoV-2 Alpha and Delta Variants during Large Nationwide Outbreak of COVID-19, Vietnam, 2021

Nguyen Thi Tam; Nguyen To Anh; Trinh Son Tung; Pham Ngoc Thach; Nguyen Thanh Dung; Van Dinh Trang; Le Manh Hung; Trinh Cong Dien; Nghiem My Ngoc; Le Van Duyet; Phan Manh Cuong; Hoang Vu Mai Phuong; Pham Quang Thai; Nguyen Le Nhu Tung; Dinh Nguyen Huy Man; Nguyen Thanh Phong; Vo Minh Quang; Pham Thi Ngoc Thoa; Nguyen Thanh Truong; Tran Nguyen Phuong Thao; Dao Phuong Linh; Ngo Tan Tai; Ho The Bao; Vo Trong Vuong; Huynh Thi Kim Nhung; Phan Nu Dieu Hong; Le Thi Phuoc Hanh; Le Thanh Chung; Nguyen Thi Thanh Nhan; Ton That Thanh; Do Thai Hung; Huynh Kim Mai; Trinh Hoang Long; Nguyen Thu Trang; Nguyen Thi Hong Thuong; Nguyen Thi Thu Hong; Le Nguyen Truc Nhu; Nguyen Thi Han Ny; Cao Thu Thuy; Le Kim Thanh; Lam Anh Nguyet; Le Thi Quynh Mai; Tang Chi Thuong; Le Hong Nga; Tran Tan Thanh; Guy Thwaites; H Rogier van Doorn; Nguyen Van Vinh Chau; Thomas Kesteman; Le Van Tan; for the OUCRU COVID-19 Research Group

doi:10.3201/eid2905.221787

. 2023 May;29(5):1002–1006. doi: 10.3201/eid2905.221787

Spatiotemporal Evolution of SARS-CoV-2 Alpha and Delta Variants during Large Nationwide Outbreak of COVID-19, Vietnam, 2021

Nguyen Thi Tam ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen To Anh ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,^12,^✉, Trinh Son Tung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Pham Ngoc Thach ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thanh Dung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Van Dinh Trang ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Manh Hung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Trinh Cong Dien ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nghiem My Ngoc ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Van Duyet ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Phan Manh Cuong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Hoang Vu Mai Phuong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Pham Quang Thai ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Le Nhu Tung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Dinh Nguyen Huy Man ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thanh Phong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Vo Minh Quang ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Pham Thi Ngoc Thoa ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thanh Truong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Tran Nguyen Phuong Thao ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Dao Phuong Linh ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Ngo Tan Tai ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Ho The Bao ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Vo Trong Vuong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Huynh Thi Kim Nhung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Phan Nu Dieu Hong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Thi Phuoc Hanh ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Thanh Chung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thi Thanh Nhan ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Ton That Thanh ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Do Thai Hung ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Huynh Kim Mai ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Trinh Hoang Long ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thu Trang ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thi Hong Thuong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thi Thu Hong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Nguyen Truc Nhu ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Thi Han Ny ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Cao Thu Thuy ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Kim Thanh ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Lam Anh Nguyet ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Thi Quynh Mai ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Tang Chi Thuong ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Hong Nga ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Tran Tan Thanh ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Guy Thwaites ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², H Rogier van Doorn ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Nguyen Van Vinh Chau ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Thomas Kesteman ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹², Le Van Tan ^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,^12,^✉; for the OUCRU COVID-19 Research Group^1,^2,^3,^4,^5,^6,^7,^8,^9,^10,^11,¹²

PMCID: PMC10124647 PMID: 37015283

Abstract

We analyzed 1,303 SARS-CoV-2 whole-genome sequences from Vietnam, and found the Alpha and Delta variants were responsible for a large nationwide outbreak of COVID-19 in 2021. The Delta variant was confined to the AY.57 lineage and caused >1.7 million infections and >32,000 deaths. Viral transmission was strongly affected by nonpharmaceutical interventions.

Keywords: COVID-19, coronavirus disease, SARS-CoV-2, severe acute respiratory syndrome coronavirus-2, coronaviruses, viruses, coronavirus disease, respiratory infections, Alpha variant, Delta variant, spatiotemporal evolution, outbreak, zoonoses, Vietnam

After successfully controlling SARS-CoV-2 transmission in 2020 (1), Vietnam experienced a large nationwide outbreak of infection with SARS-CoV-2 in 2021. This outbreak was characterized by 2 distinct phases: January–April, with 1,632 infections and no deaths, and May–December, with 1,727,398 infections and 32,359 deaths (2).

Genomic surveillance has been one of the top priorities of the World Health Organization and has generated major insights into the spatiotemporal evolution of SARS-CoV-2 (3), which are critical for pandemic response. However, most of the studies published about genetic evolution of SARS-CoV-2 are based on datasets from high-income countries with relatively open borders (4–6), and little is known about the transmission dynamics of SARS-CoV-2 in countries such as Vietnam where strict nonpharmaceutical interventions were implemented. We analyzed the spatiotemporal evolution of SARS-CoV-2 in Vietnam during 2021 and mapped patterns of viral evolution and diffusion against the public health measures implemented during the study period.

The Study

The study was conducted at the National Hospital for Tropical Diseases in Hanoi, Vietnam, and the Hospital for Tropical Diseases in Ho Chi Minh City, Vietnam. Both are tertiary referral hospitals for COVID-19 patients in northern (hospital in Hanoi) and southern (hospital in Ho Chi Minh City) Vietnam. The laboratories of the 2 hospitals were responsible for SARS-CoV-2 diagnosis and sequencing in Vietnam. We compiled detailed study methods, including public health measures (Appendix Figure 1), and demographic features of study participants (Table).

Table. Demographics of study participants for spatiotemporal evolution of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021*.

Characteristic	No. sequences, n = 1,303	Alpha, n = 74	AY.57, n = 1,212
Age, y
Median (Q1‒Q3)	43 (29‒61)	35 (30–55)	44 (29‒61)
Missing	38 (2.9)	31 (41.9)	2 (0.2)
Sex
M	689 (52.9)	22 (29.7)	661 (54.5)
F	578 (44.4)	21 (28.4)	551 (45.5)
Unknown	36 (2.8)	31 (41.9)
Region
Central	120 (9.2)	24 (32.4)	94 (7.8)
Northern	504 (38.7)	44 (59.5)	450 (37.1)
Southern	679 (52.1)	6 (8.1)	668 (55.1)

Open in a new tab

*Values are no. (%) unless indicated otherwise. Characteristics of A.23.1 variant‒infected cases were previously reported (7). Q, quartile.

We selected 1,365 nasopharyngeal throat swab specimens for whole-genome sequencing and obtained 1,303 complete genome sequences. We detected no recombinants. Most obtained sequences belonged to Delta variant (93.8%, n = 1,222), followed by Alpha (5.7%, n = 74), A.23.1 (0.4%, n = 5), and B.1.637 (0.2%, n = 2) variants. Of the Delta sequences, 1,212 (99.2%) were assigned to AY.57 lineage by PANGO lineage (8). The remaining were assigned to AY.23 and AY.79 (n = 3 each), AY.6, AY.38, AY.85, and B.1.617.2 (n = 1 each).

We temporally documented the Alpha and A.23.1 sequences during January‒May 2021. We detected the first 3 Delta sequences, including 2 AY.57 and 1 B.1.617.2, in late April 2021. From June on, Delta was the only variant detected, coinciding with an upsurge in the number of infections and deaths during the 2021 outbreak (Appendix Figure 2).

Maximum-likelihood phylogenetic analysis of Alpha variant sequences showed that they were closely related to the contemporary sequences detected in the region and clustered into 4 major groups, corresponding to the sporadic community transmission clusters detected in northern, central, and southern Vietnam in early 2021 (Figure 1). This finding suggested that multiple importations and exportations of the Alpha variant into Vietnam occurred during January‒May 2021.

Maximum-likelihood tree of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021. Complete coding sequences of Alpha variant viruses circulating in Vietnam in 2021 are shown. Phylogenetic clusters were named accordingly to community clusters recorded during the study period shown in Appendix Figure 1). Numbers along branches are bootstrap values. Cluster II was linked with a traveler from Japan (Appendix Figure 1). Outgroup was the SARS-CoV-2 wild-type strain (GenBank accession no. NC_0455122).

Because of the dominance of the AY.57 lineage, and the small number of AY.57 sequences reported outside Vietnam, and especially in the nearby region (Cambodia, n = 5; Thailand, n = 5; Laos, n = 0; Singapore, n = 5), we focused our phylogeographic analysis on the 1,212 Delta AY.57/1.303 sequences obtained from Vietnam. After we removed identical, low-quality, and outlier sequences, as suggested by TempEst software, (https://tempest-solutions.com), 748 non-identical sequences were available for analysis.

Results confirmed that AY.57 viruses were introduced into the northeastern region in early 2021 (Figure 2) probably by a single introduction event (Appendix Figure 4). The estimated time to the most recent common ancestor was March 14, 2021 (95% CI February 22, 2021‒April 8, 2021), shortly after the discovery of the Delta variant in November 2020. In the following months, the northeastern and Red River delta regions then acted as a source seeding the virus to neighboring and southeastern provinces, with limited viral dispersal between provinces/cities (Figure 2). During July‒December 2021, the southeastern region was the main source, seeding the virus back to the northern region and the rest of Vietnam. In addition, we observed the establishment of multiple localized clusters of AY.57 lineage elsewhere in the southcentral coastal region and the Red River delta (Figure 2).

Spatiotemporal evolution of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021. Maximum clade credibility tree illustrates the phylogeography of AY.57 lineage in Vietnam in 2021, Branches are color-coded according to locations of sampling shown on map. Numbers along branches are bootstrap values. Posterior probabilities >0.8% and state probabilities >75% (black circles) are indicated at all nodes.

A Bayesian Skyride showed a sharp increase in genetic diversity during April‒August 2021 (Figure 3, panel A), reflecting the expansion of the AY.57 lineage across the country, paralleling the start of the large nationwide outbreak from May onward (Appendix Figures 1, 2). In the following months, the viral population size remained relative stable, despite some fluctuations in the number of viral sequences obtained (Figure 3, panel B), followed by a slight decrease in the genetic diversity during November. The estimated mean of the nonsynonymous to synonymous substitution (dN/dS) value was 0.86, albeit it varied across the genomes (Appendix Table 1), and the evolutionary rate of AY.57 coding sequences was 5.29 × 10⁻⁴ substitutions/site/year (95% CI 4.966 × 10⁻⁴ to 5.639 × 10⁻⁴ substitutions/site/year).

Genetic diversity and distribution of SARS-CoV-2 AY.57 lineage during large nationwide outbreak of COVID-19, Vietnam, 2021. A) Bayesian skyride plot illustrating the relative genetic diversity of AY.57 lineage in Vietnam during 2021. Purple shading indicates 95% highest posterior density interval. B) Distribution of the number of AY.57 sequences used for analysis over the study period.

Conclusions

We showed that the Alpha and especially Delta variants were the main causes of SARS-CoV-2 outbreaks of >1.7 million infections and >32,000 deaths in Vietnam during 2021. The Alpha variant was introduced into Vietnam during early 2021 by different importation events but only caused sporadic community outbreaks until May, when a second wave associated with the Delta variant predominated from June on. The viruses of the Delta variant were confined to AY.57 lineage and were responsible for the major wave in 2021, probably by a single introduction event. Viral movement between provinces was not apparent. During the study period, nearly 200 sublineages of the Delta variant were documented worldwide (9), and in other countries, such as the United Kingdom and the United States, where use of nonpharmaceutical measures was relaxed, viral dispersal across the localities was more apparent (10,11). The rigorous containment approach applied in Vietnam in 2021, with limited domestic travels and tight border controls, was probably the key factor determining the localization of a single AY.57 lineage in Vietnam and its limited dispersal across the country.

The sharp increase in the relative genetic diversity of the AY.57 lineage during April‒July 2021 marked the start of the nationwide outbreak in subsequent months despite in-country lockdown measures. Although nonpharmaceutical interventions were sufficient to prevent uncontrolled community transmission in 2020 (1), they were not sufficient after introduction of the Delta variant. This finding was probably caused by the much higher transmissibility of the Delta variant and the immunologically naive population in Vietnam at the time. During April‒July 2021, only <1% of 97 million persons in Vietnam were vaccinated against SARS-CoV-2 (12).

Although our estimated evolutionary rate was AY.57-lineage specific, the result was within the range of previously estimated values for the Delta variant more broadly (10; N. Benazi, Institut Pasteur of Algeria, and S. Bounab, University of M’sila, pers. comm., email, 2023 Mar 1). This finding points to a fast evolution of the AY.57 lineage in Vietnam during the study. Although the role of population immune landscapes in shaping the evolution of SARS-CoV-2 merits further research, a recent report showed that vaccines had played a role in selective adaptation of the SARS-CoV-2 Delta variant (13).

The potential bias toward our referral-hospital based sampling approach represents a limitation of our study, which might have failed to comprehensively capture the genetic diversity of the pathogen. However, this limitation was probably modest given that our results are consistent with sequences uploaded to GISAID (https://www.gisaid.org) (9).

In conclusion, we report how rigorous public health measures in Vietnam influenced the introduction and spread of the Alpha and Delta variants during the large nationwide outbreak of COVID-19 in 2021. Genomic surveillance is critical to inform pandemic response.

Appendix

Additional information on spatiotemporal evolution of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021.

22-1787-Techapp-s1.pdf^{(2.2MB, pdf)}

Acknowledgments

We thank Le Nguyen Minh Hoa and technicians at Department of Microbiology and Molecular, National Hospital for Tropical Diseases for collecting swab samples and initial testing of SARS-CoV-2 diagnostics; the OUCRU team for supporting whole-genome sequencing and providing data entry; data contributors and their laboratories for obtaining specimens for this study; and laboratories that submitted and shared their generated genetic sequences and metadata via GISAID, on which this research is based.

Genomic surveillance was supported by the Wellcome Trust (222574/Z/21/Z). L.V.T. and G.T. are supported by the Wellcome Trust of Great Britain (204904/Z/16/Z and 106680/B/14/Z, respectively).

Members of the OUCRU COVID-19 research group: Mary Chambers, Marc Choisy, Dong Huu Khanh Trinh, Dong Thi Hoai Tam, Du Hong Duc, Dung Vu Tien Viet, Jaom Fisher, Barney Flower, Ronald Geskus, Hang Vu Thi Kim, Ho Quang Chanh, Ho Thi Bich Hai, Ho Van Hien, Hung Vu Bao, Huong Dang Thao, Huynh le Anh Huy, Huynh Ngan Ha, Huynh Trung Trieu, Huynh Xuan Yen, Evelyne Kestelyn, Thomas Kesteman, Lam Anh Nguyet, Katrina Lawson, Leigh Jones, Le Kim Thanh, Le Dinh Van Khoa, Le Thanh Hoang Nhat, Le Van Tan, Sonia Odette Lewycka, Lam Minh Yen, Le Nguyen Truc Nhu, Le Thi Hoang Lan, Nam Vinh Nguyen, Ngo Thi Hoa, Nguyen Bao Tran, Nguyen Duc Manh, Nguyen Hoang Yen, Nguyen Le Thao My, Nguyen Minh Nguyet, Nguyen To Anh, Nguyen Thanh Ha, Nguyen Than Ha Quyen, Nguyen Thanh Ngoc, Nguyen Thanh Thuy Nhien, Nguyen Thi Han Ny, Nguyen Thi Hong Thuong, Nguyen Thi Hong Yen, Nguyen Thi Huyen Trang, Nguyen Thi Kim Ngoc, Nguyen Thi Kim Tuyen, Nguyen Thi Ngoc Diep, Nguyen Thi Phuong Dung, Nguyen Thi Tam, Nguyen Thi Thu Hong, Nguyen Thu Trang, Nguyen Thuy Thuong Thuong, Nguyen Xuan Truong, Nhung Doan Phuong, Ninh Thi Thanh Van, Ong Phuc Thinh, Pham Ngoc Thanh, Phan Nguyen Quoc Khanh, Phung Ho Thi Kim, Phung Khanh Lam, Phung Le Kim Yen, Phung Tran Huy Nhat, Motiur Rahman, Thuong Nguyen Thi Huyen, Guy Thwaites, Louise Thwaites, Tran Bang Huyen, Tran Dong Thai Han, Tran Kim Van Anh, Tran Minh Hien, Tran Phuong Thao, Tran Tan Thanh, Tran Thi Bich Ngoc, Tran Thi Hang, Tran Tinh Hien, Trinh Son Tung, H. Rogier van Doorn, Jennifer Van Nuil, Celine Pascale Vidaillac, Vu Thi Ngoc Bich, Vu Thi Ty Hang, and Sophie Yacoub. Members of the HTD COVID-19 research group: Nguyen Van Vinh Chau, Nguyen Thanh Dung, Le Manh Hung, Huynh Thi Loan, Nguyen Thanh Truong, Nguyen Thanh Phong, Dinh Nguyen Huy Man, Nguyen Van Hao, Duong Bich Thuy, Nghiem My Ngoc, Nguyen Phu Huong Lan, Pham Thi Ngoc Thoa, Tran Nguyen Phuong Thao, Tran Thi Lan Phuong, Le Thi Tam Uyen, Tran Thi Thanh Tam, Bui Thi Ton That, Huynh Kim Nhung, Ngo Tan Tai, Tran Nguyen Hoang Tu, Vo Trong Vuong, Dinh Thi Bich Ty, Le Thi Dung, Thai Lam Uyen, Nguyen Thi My Tien, Ho Thi Thu Thao, Nguyen Ngoc Thao, Huynh Ngoc Thien Vuong, Huynh Trung Trieu, Pham Ngoc Phuong Thao, and Phan Minh Phuong. Members of the EOCRU COVID-19 research group: Andy Bachtiar, J. Kevin Baird, Fitri Dewi, Ragil Dien, Bimandra A. Djaafara, Iqbal E. Elyazar, Raph H. Hamers, Winahyu Handayani, Livia N. Kurniawan, Ralalicia Limato, Cindy Natasha, Nunung Nuraeni, Khairunisa Puspatriani, Mutia Rahadjani, Atika Rimainar, Saraswati Shankar, H. Anuraj, Henry Suhendra, Ida Sutrisni, Ayu Suwarti, Nicolas Tarino, Diana Timoria, and Fitri Wulandari. Members of the OUCRU-NP COVID-19 research group: Buddha Basnyat, Manish Duwal, Amit Gautum, Abhilasha Karkey, Niharika Kharel, Aakriti Pandey, Samia Rijal, Suchita Shrestha, Pratibha Thapa, Summita Udas.

Biography

Dr. Tam is a postdoctoral scientist at the Oxford University Clinical Research Unit, Hanoi, Vietnam. Her primary research interests are genomic surveillance of SARS-CoV-2 variants emerging in Vietnam since 2020, and situation and molecular mechanisms of antimicrobial drug resistance for bacterial pathogens in Vietnam.

Footnotes

Suggested citation for this article: Tam NT, Anh NT, Tung TS, Thach PN, Dung NT, Trang VD, et al. Spatiotemporal evolution of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021. Emerg Infect Dis. 2023 May [date cited]. https://doi.org/10.3201/eid2905.221787

These authors contributed equally to this article.

Members of the working group are shown at the end of this article.

References

1.Van Tan L. COVID-19 control in Vietnam. Nat Immunol. 2021;22:261. 10.1038/s41590-021-00882-9 [DOI] [PubMed] [Google Scholar]
2.World Health Organization. COVID-19 in Viet Nam Situation report 101, 2022. [cited 2022 Oct 24]. https://www.who.int/vietnam/internal-publications-detail/covid-19-in-viet-nam-situation-report-101
3.Attwood SW, Hill SC, Aanensen DM, Connor TR, Pybus OG. Phylogenetic and phylodynamic approaches to understanding and combating the early SARS-CoV-2 pandemic. Nat Rev Genet. 2022;23:547–62. 10.1038/s41576-022-00483-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
4.du Plessis L, McCrone JT, Zarebski AE, Hill V, Ruis C, Gutierrez B, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. Establishment and lineage dynamics of the SARS-CoV-2 epidemic in the UK. Science. 2021;371:708–12. 10.1126/science.abf2946 [DOI] [PMC free article] [PubMed] [Google Scholar]
5.da Silva Filipe A, Shepherd JG, Williams T, Hughes J, Aranday-Cortes E, Asamaphan P, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland. Nat Microbiol. 2021;6:112–22. 10.1038/s41564-020-00838-z [DOI] [PubMed] [Google Scholar]
6.Lemey P, Ruktanonchai N, Hong SL, Colizza V, Poletto C, Van den Broeck F, et al. Untangling introductions and persistence in COVID-19 resurgence in Europe. Nature. 2021;595:713–7. 10.1038/s41586-021-03754-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
7.Chau NVV, Hong NTT, Ngoc NM, Anh NT, Trieu HT, Nhu LNT, et al. ; for OUCRU COVID-19 research group. Rapid whole-genome sequencing to inform COVID-19 outbreak response in Vietnam. J Infect. 2021;82:276–316. 10.1016/j.jinf.2021.03.017 [DOI] [PMC free article] [PubMed] [Google Scholar]
8.Github. Co-lineages/pangolin [cited 2023 Mar 7]. https://github.com/cov-lineages/pangoli
9.Spectrum COV. Detect and analyze variants of SARS-CoV-2 [cited 2023 Mar 7]. https://cov-spectrum.org/explore/Vietnam/AllSamples/Past6M
10.Eales O, Page AJ, de Oliveira Martins L, Wang H, Bodinier B, Haw D, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2. BMC Infect Dis. 2022;22:647. 10.1186/s12879-022-07628-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
11.McCrone JT, Hill V, Bajaj S, Pena RE, Lambert BC, Inward R, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. Context-specific emergence and growth of the SARS-CoV-2 Delta variant. Nature. 2022;610:154–60. 10.1038/s41586-022-05200-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
12.Our World in Data. Vietnam: coronavirus pandemic country profile [cited 2023 Mar 7]. https://ourworldindata.org/coronavirus/country/vietnam
13.Duerr R, Dimartino D, Marier C, Zappile P, Levine S, Francois F, et al. Clinical and genomic signatures of SARS-CoV-2 Delta breakthrough infections in New York. EBioMedicine. 2022;82:104141. 10.1016/j.ebiom.2022.104141 [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Appendix

Additional information on spatiotemporal evolution of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021.

22-1787-Techapp-s1.pdf^{(2.2MB, pdf)}

[R1] 1.Van Tan L. COVID-19 control in Vietnam. Nat Immunol. 2021;22:261. 10.1038/s41590-021-00882-9 [DOI] [PubMed] [Google Scholar]

[R2] 2.World Health Organization. COVID-19 in Viet Nam Situation report 101, 2022. [cited 2022 Oct 24]. https://www.who.int/vietnam/internal-publications-detail/covid-19-in-viet-nam-situation-report-101

[R3] 3.Attwood SW, Hill SC, Aanensen DM, Connor TR, Pybus OG. Phylogenetic and phylodynamic approaches to understanding and combating the early SARS-CoV-2 pandemic. Nat Rev Genet. 2022;23:547–62. 10.1038/s41576-022-00483-8 [DOI] [PMC free article] [PubMed] [Google Scholar]

[R4] 4.du Plessis L, McCrone JT, Zarebski AE, Hill V, Ruis C, Gutierrez B, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. Establishment and lineage dynamics of the SARS-CoV-2 epidemic in the UK. Science. 2021;371:708–12. 10.1126/science.abf2946 [DOI] [PMC free article] [PubMed] [Google Scholar]

[R5] 5.da Silva Filipe A, Shepherd JG, Williams T, Hughes J, Aranday-Cortes E, Asamaphan P, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. Genomic epidemiology reveals multiple introductions of SARS-CoV-2 from mainland Europe into Scotland. Nat Microbiol. 2021;6:112–22. 10.1038/s41564-020-00838-z [DOI] [PubMed] [Google Scholar]

[R6] 6.Lemey P, Ruktanonchai N, Hong SL, Colizza V, Poletto C, Van den Broeck F, et al. Untangling introductions and persistence in COVID-19 resurgence in Europe. Nature. 2021;595:713–7. 10.1038/s41586-021-03754-2 [DOI] [PMC free article] [PubMed] [Google Scholar]

[R7] 7.Chau NVV, Hong NTT, Ngoc NM, Anh NT, Trieu HT, Nhu LNT, et al. ; for OUCRU COVID-19 research group. Rapid whole-genome sequencing to inform COVID-19 outbreak response in Vietnam. J Infect. 2021;82:276–316. 10.1016/j.jinf.2021.03.017 [DOI] [PMC free article] [PubMed] [Google Scholar]

[R8] 8.Github. Co-lineages/pangolin [cited 2023 Mar 7]. https://github.com/cov-lineages/pangoli

[R9] 9.Spectrum COV. Detect and analyze variants of SARS-CoV-2 [cited 2023 Mar 7]. https://cov-spectrum.org/explore/Vietnam/AllSamples/Past6M

[R10] 10.Eales O, Page AJ, de Oliveira Martins L, Wang H, Bodinier B, Haw D, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. SARS-CoV-2 lineage dynamics in England from September to November 2021: high diversity of Delta sub-lineages and increased transmissibility of AY.4.2. BMC Infect Dis. 2022;22:647. 10.1186/s12879-022-07628-4 [DOI] [PMC free article] [PubMed] [Google Scholar]

[R11] 11.McCrone JT, Hill V, Bajaj S, Pena RE, Lambert BC, Inward R, et al. ; COVID-19 Genomics UK (COG-UK) Consortium. Context-specific emergence and growth of the SARS-CoV-2 Delta variant. Nature. 2022;610:154–60. 10.1038/s41586-022-05200-3 [DOI] [PMC free article] [PubMed] [Google Scholar]

[R12] 12.Our World in Data. Vietnam: coronavirus pandemic country profile [cited 2023 Mar 7]. https://ourworldindata.org/coronavirus/country/vietnam

[R13] 13.Duerr R, Dimartino D, Marier C, Zappile P, Levine S, Francois F, et al. Clinical and genomic signatures of SARS-CoV-2 Delta breakthrough infections in New York. EBioMedicine. 2022;82:104141. 10.1016/j.ebiom.2022.104141 [DOI] [PMC free article] [PubMed] [Google Scholar]

PERMALINK

Spatiotemporal Evolution of SARS-CoV-2 Alpha and Delta Variants during Large Nationwide Outbreak of COVID-19, Vietnam, 2021

Nguyen Thi Tam

Nguyen To Anh

Trinh Son Tung

Pham Ngoc Thach

Nguyen Thanh Dung

Van Dinh Trang

Le Manh Hung

Trinh Cong Dien

Nghiem My Ngoc

Le Van Duyet

Phan Manh Cuong

Hoang Vu Mai Phuong

Pham Quang Thai

Nguyen Le Nhu Tung

Dinh Nguyen Huy Man

Nguyen Thanh Phong

Vo Minh Quang

Pham Thi Ngoc Thoa

Nguyen Thanh Truong

Tran Nguyen Phuong Thao

Dao Phuong Linh

Ngo Tan Tai

Ho The Bao

Vo Trong Vuong

Huynh Thi Kim Nhung

Phan Nu Dieu Hong

Le Thi Phuoc Hanh

Le Thanh Chung

Nguyen Thi Thanh Nhan

Ton That Thanh

Do Thai Hung

Huynh Kim Mai

Trinh Hoang Long

Nguyen Thu Trang

Nguyen Thi Hong Thuong

Nguyen Thi Thu Hong

Le Nguyen Truc Nhu

Nguyen Thi Han Ny

Cao Thu Thuy

Le Kim Thanh

Lam Anh Nguyet

Le Thi Quynh Mai

Tang Chi Thuong

Le Hong Nga

Tran Tan Thanh

Guy Thwaites

H Rogier van Doorn

Nguyen Van Vinh Chau

Thomas Kesteman

Le Van Tan

Abstract

The Study

Table. Demographics of study participants for spatiotemporal evolution of SARS-CoV-2 Alpha and Delta variants during large nationwide outbreak of COVID-19, Vietnam, 2021*.

Figure 1.

Figure 2.

Figure 3.

Conclusions

Acknowledgments

Biography

Footnotes

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases