
correspondence The lag in SARS-CoV-2 genome submissions to GISAID To the Editor — Genomic surveillance krisp.org.za/ngs-sa/ngs-sa_network_for_ genomes each, which is 1.5% and 9.3% of of the evolving SARS-CoV-2 strains is genomic_surveillance_south_africa/) and their respective positive samples. India, an important tool for helping control the SPHERES (United States; https://www.cdc. being the second-largest country on the pandemic1. For efficient surveillance, the gov/coronavirus/2019-ncov/covid-data/ basis of both total population and known first major requirement for analysis of how spheres.html). Even so, although an COVID-19 cases, has sequenced a mere the virus is evolving and spreading is the increasing fraction of COVID-19 samples 0.05% of the collected samples. On average, availability of all sequenced genomes on are being sequenced9, an equally important African, Asian and South American an open-access platform that is accessible issue is how soon the sequences are being countries have sequenced a mere 0.36%, to researchers worldwide. Therefore, submitted to GISAID. Rapid submission 0.21% and 0.07% of their total COVID-19 soon after researchers became aware of is important as it enables the international samples, respectively, whereas this number COVID-19, toward the end of 2019, the community to analyze the variants is 1.9%, 1.4% and 37% for European, Global Initiative on Sharing All Influenza emerging around the world quickly North American and Oceania countries. Data (GISAID), an existing platform for and provide actionable information to Population-wise, most of the European sharing influenza virus sequences, began governments. countries, the United States, Israel (Asia) receiving deposits of SARS-CoV-2 genome Our statistical analysis (Fig. 1, and the island of Réunion have sequenced sequences. Here we report an analysis of Supplementary Fig. 1 and Supplementary samples from over 1,000 people per the median collection to submission time Tables 1 and 2) for the 1,718,035 million population (ppmp). Among (CST) lag for SARS-CoV-2 sequences to SARS-CoV-2 strains submitted to GISAID countries with over 100 million population, GISAID on a country-by-country basis. (as of 27 May 2021) has determined that including Brazil (50 ppmp), India Our results suggest that researchers in the CST lag per strain ranges from 1 day (11 ppmp), Indonesia (6 ppmp), Nigeria United Kingdom are the fastest, logging to over 1 year. We have also calculated (4 ppmp) and Pakistan (1 ppmp), only sequences in a median time of 16 days, the median CST lag for each country. the United States (1,497 ppmp) and Japan which is not only more than 5 times as Examining the median CST lag values for (297 ppmp) have sequenced over 100 ppmp. fast as the upload times of sequences countries that have sequenced over 1,000 Cumulatively, African, Asian and South originating from industrial countries SARS-CoV-2 genomes, we note that the American countries have sequenced only such as Japan or Canada, but also 18 CST lag from the United Kingdom is the 14, 21 and 49 ppmp whereas this number times as fast as that of Qatar, among shortest (namely, 16 days for over 417,000 is 1,198, 948 and 607 ppmp for European, the countries that have sequenced genomes). This is almost a week faster than North American and Oceania countries over 1,000 genomes. the CST lags of 25 and 26 days for over (Supplementary Table 2). As of now, GISAID is the largest 590,000 and 498,000 genomes in the rest of Several reasons may explain the delay open-access portal, hosting the genome Europe and the United States, respectively. in sequence submissions to GISAID. sequences and related epidemiological For Canada, the CST lag is over five times Submission times are based on (i) the and clinical data of more than 1.7 million as long: 88 days for over 44,000 genomes. time taken from sample collection from SARS-CoV-2 strains. Thanks to ongoing Among the countries of Oceania, the CST a patient to RNA isolation in the lab and genomic surveillance using GISAID data, lag for New Zealand is 40 days for over its dispatch to the sequencing center and several new SARS-CoV-2 variants, such as 1,000 genomes, whereas for Australia it is (ii) the time from RNA sample arrival B.1.1.7 (Alpha; first identified in the United 51 days for over 17,000 genomes. In Asia, at the sequencing center to uploading Kingdom), B.1.351 (Beta; first identified the median CST lag is 72 days for over of the sequence to GISAID. Countries in South Africa), B.1.1.28 (Gamma; P.1, 89,000 genomes, with Singapore having the like the United Kingdom and Denmark first identified in Brazil), B.1.617.2 (Delta; shortest lag, 26 days for 2,405 genomes, with a short median CST lag have strong first identified in India), B.1.617.1 (Kappa; and Qatar the longest, 289 days for 2,298 public health systems, allowing efficient first identified in India), P.3 (Theta; first genomes. India’s median CST lag is 57 sample and metadata collection and identified in the Philippines), and B.1.427 days for 15,614 genomes whereas Japan, smoother coordination between the sample and B.1.429 (Epsilon; first identified in the which has sequenced the most genomes collection center, the RNA isolation lab United States), have been identified2–5. This in Asia, has taken 79 days for over 37,000 and the sequencing lab. Countries without information has been used to update public genomes. For South American countries, such a strong system are at a disadvantage health policies for the control of COVID-19 the median lag is 61 days for over 18,000 and may face additional logistical problems infections6,7. genomes, whereas countries in Africa in sample and metadata collection and Considering the benefits of genomic have taken 50 days for over 7,000 genomes shipping because of lockdown-related surveillance6,8, scientists have pressured (Supplementary Table 2). restrictions. Several countries might countries to increase their sequencing Coming to the rate of sequencing, have a shortage of labs that can handle capacity, and this has led to several top-performing countries Iceland, Australia, COVID-19 samples or might have an initiatives, such as COG-UK (United New Zealand and Denmark have sequenced overly centralized system wherein only Kingdom; https://www.cogconsortium. ~77%, 59%, 39% and 35% of their positive a few labs are authorized to handle such uk/), INSA-COG (India; https://pib.gov.in/ samples, respectively (Supplementary samples, causing a delay in sequencing PressReleseDetailm.aspx?PRID=1684782), Table 1). The United States and United and submission. A paucity of funds or NGS-SA (South Africa; http://www. Kingdom have sequenced over 400,000 restrictions on importing reagents and 1058 NATURE BIOTECHNOLOGY | VOL 39 | SEPTEMBER 2021 | 1055–1065 | www.nature.com/naturebiotechnology correspondence 525 Compact area 150 125 100 75 50 Collection to submission time lag (CSTlag) 25 Continent 0 Europe Italy Peru India Chile Israel Brazil Qatar Spain China Asia Japan Tur key France Russia Ireland Poland Latvia Austria Mexico Croatia Iceland Finland Greece Estonia Norway Sweden Belgium Bulgaria Portugal Reunion Slovakia Slovenia Thailand Australia Canada Lithuania Denmark Germany North America Colombia Argentina Indonesia Singapore Philippines Hong Kong Switzerland Bangladesh Netherlands South Africa South Korea South America Luxembourg New Zealand New United States Czech Republic Czech Oceania United Kingdom Africa United Arab Emirates United Arab 0 5,000 10,000 15,000 20,000 (27 May 2021) (27 May 25,000 30,000 Genomes submitted to GISAID Compact area 500,000 Fig. 1 | Violin plot illustrating the CST lag values for the 54 countries that have sequenced over 1,000 genomes. The box plot inside the violin plot depicts the median CST lag per country. Outlier CST lag entries are not shown. Country name is color-coded according to continent. We have also graphed the relative distribution of the number of genome sequences submitted by each country as a bar plot. equipment would also add to the delay. The listed above are known to have been true in particularly sensitive to the issue of virulent use of older sequencing technologies that India, for instance, and are being resolved10,11. strains being named after their countries. are low throughput and more expensive Sometimes, even after rapid sequencing, The WHO initiative of renaming variants per sample would complicate matters genomes may not be promptly uploaded with Greek letters may help resolve this further. to GISAID, and there may be several issue5. Finally, in many countries, significant Most of the countries with a short CST reasons for that. First, the importance of bureaucratization or political interference lag are industrialized nations that are likely genomic surveillance may not have been at various steps, from sample collection to have strong linkages between the clinical well understood, especially in the early to uploading sequences to GISAID, can and scientific establishments, although Japan months of the pandemic. Second, there add to the delay. In several countries— and Canada are outliers. This is not always may be a wish to withhold information, including the United States—where most of so for other countries. Some of the countries to publish or patent first. Although there the testing and sampling is carried out by with a longer CST lag have a less developed is a general understanding that scientists private diagnostic labs, there is no financial public health system. They might also have do not publish work based on others’ data incentive to share data, and the labs there had to establish new collaborations and unless the latter are acknowledged or have may prefer to discard samples rather than institutional arrangements to help deal with already published on them, there have been pay for their storage or shipping.
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