International Journal of Infectious Diseases 104 (2021) 139–149

Contents lists available at ScienceDirect

International Journal of Infectious Diseases

journal homepage: www.elsevier.com/locate/ijid

Molecular epidemiology of COVID-19 in Oman: A molecular and

surveillance study for the early transmission of COVID-19 in the
country
Samira Al-Mahruqia , Adil Al-Wahaibia , Abdul Latif Khanb, Amina Al-Jardania, Sajjad Asafb,
Hanan Alkindia, Samiha Al-Kharusia, Ahmed N. Al-Rawahib, Ahmed Al-Rawahib,
Majid Al-Salmanib, Intisar Al-Shukria , Aisha Al-Busaidia, Seif Salem Al-Abria,* ,
Ahmed Al-Harrasib,*
a
Directorate General for Disease Surveillance and Control, Ministry of Health, Sultanate of Oman, P.O. Box 393, PC 100 Muscat, Oman
b
Natural and Medical Sciences Research Center, University of Nizwa, P.O. Box 33, PC 616 Nizwa, Oman

A R T I C L E I N F O A B S T R A C T

Article history: Background: Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) has been proven to be lethal
Received 15 November 2020 to human health, which affects almost every corner of the world. The objectives of this study were to add
Received in revised form 13 December 2020 context to the global data and international genomic consortiums, and to give insight into the efficiency
Accepted 17 December 2020
of the contact tracing system in Oman.
Methods: We combined epidemiological data and whole-genome sequence data from 94 samples of
Keywords: SARS-CoV-2 in Oman to understand the origins, genetic variation, and transmissibility. The whole-
SARS-CoV-2
genome size of sequence data was obtained through a customized SARS-COV-2 research panel. Amplifier
COVID-19 epidemiology
Phylogenomic analysis
methods ranged from 26 Kbp to 30 Kbp and were submitted to GISAID.
Clade Findings: The study found that P323L (94.7%) is the most common mutation, followed by D614G (92.6%)
Mutation Spike protein mutation. A unique mutation, I280V, was first reported in Oman and was associated with a
Oman rare lineage, B.1.113 (10.6%). In addition, the study revealed a good agreement between genetic and
epidemiological data.
Interpretation: Oman’s robust surveillance system was very efficient in guiding the outbreak investigation
processes in the country, the study illustrates the future importance of molecular epidemiology in
leading the national response to outbreaks and pandemics.
© 2020 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-
nd/4.0/).

Introduction coronavirus disease-2019 (COVID-19) have been reported, which

caused more than 1.5 million deaths (WHO 2020). Coronavirus,
The severe acute respiratory syndrome coronavirus-2 (SARS- subfamily Coronavirinae from family Coronaviridae, comprises a
CoV-2) (Paules et al., 2020; Wu et al., 2020) outbreak began in large group of viruses that have been mainly associated with birds
Wuhan, Hubei province, China in late December 2019 and spread and mammals (Khan and McIntosh, 2005; Fehr and Perlman, 2015;
globally with extraordinarily high rates of morbidity and mortality. Paules et al., 2020). The subfamily includes four genera:
As of December 9, 2020, more than 67.5 million confirmed cases of Alphacoronavirus, Betacoronavirus, Gammacoronavirus, and Delta-
coronavirus.
The coronaviruses were first identified and characterized before
the 1960s and were attributed to cause a disease of the respiratory
* Corresponding authors. system (Khan and McIntosh, 2005; Paules et al., 2020). SARS-CoV-2
E-mail addresses: [email protected]
has spread among humans to cause catastrophic devastation in
( [email protected] (A. Al-Wahaibi), [email protected] (A.L. Khan),
[email protected] (A. Al-Jardani), [email protected] (S. Asaf), health systems and economies. Given the possible high mutation
[email protected] (H. Alkindi), [email protected] (S. Al-Kharusi), rate of RNA viruses as compared to DNA viruses, it was not
[email protected] (A.N. Al-Rawahi), [email protected] unexpected that the viral genome of SARS-CoV-2 would mutate
(A. Al-Rawahi), [email protected] (M. Al-Salmani),
more rapidly, which should allow to track the spread of the virus
[email protected] (I. Al-Shukri), [email protected] (A. Al-Busaidi),
[email protected] (S.S. Al-Abri), [email protected] (A. Al-Harrasi). (Grubaugh et al., 2019). However, with confirmed cases exceeding

https://doi.org/10.1016/j.ijid.2020.12.049
1201-9712/© 2020 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
S. Al-Mahruqi, A. Al-Wahaibi, A.L. Khan et al. International Journal of Infectious Diseases 104 (2021) 139–149

46.5 million, it has become difficult to track individual transmis- Changsha, China) was used in accordance with the manufacturer’s
sion chains due to the small size of sequences, notwithstanding instructions. The assay targets two genomic regions of the SARS-
more than 147 thousand whole-genome sequences, which have CoV-2 (N and ORF1ab). All samples included in the study had a
been deposited in GISAID, an open access global science initiative, cycle threshold (Ct) value of the gene target of less than 30.
as of October 23, 2020 (GISAID, 2020). Another striking feature of SuperScript VILO cDNA Synthesis Kit (Thermo Fisher, USA) was
coronaviruses, when compared with other RNA viruses, is the used to reverse transcribe the SARS-CoV RNA with the qPCR
likelihood to mutate slowly due to their ability to proofread; a fact program (42  C for 30 min, 85  C for 5 min, and hold on 10  C). To
accounted for 3’ to 5’ exoribonuclease (Minskaia et al., 2006). It has ensure enough cDNA content for NGS workflow, we requantified it
been reported that the estimated mutation rate of SARS-CoV-2 is on Qubit 3.0 fluorometer (Thermo Fisher Scientific, Waltham, MA,
0.71–1.40
10–3 (Hill and Rambaut, 2020). USA). The cDNA (60 ng/ul) was used to prepare libraries with Ion
The first confirmed cases of COVID-19 was reported in Oman on Xpress barcodes (Thermo Fisher Scientific, Waltham, MA, USA)
24 February of two Omani nationals who returned from a visit to through Ion AmpliSeq Library Kit Plus and predefined Ion
Iran. Initially, a steady increase in the number of imported AmpliSeq SARS-CoV-2 Research Panel (Thermo Fisher Scientific,
confirmed cases was observed in the following weeks, with the Waltham, MA, USA). The panel provides 99% coverage to viral
first suspected case of local transmission reported on March 23, genomes with fewer copy numbers and consists of two primer
2020 in Mutrah, a city within Muscat, the capital of Oman (Al pools comprising 237 amplicons of SARS-CoV-2 genomes. The
Wahaibi et al., 2020). To date, the number of infected cases has panel comprises five additional primer pairs that target human
increased to more than 115,000 and approximately 1200 deaths expression control. Workflow according to manufacturer guide-
(Ministry of Health, Oman, 2020) were recorded. The cases lines was used to prepare libraries and quantify, was template-
continue to increase up to 400 infections daily. enriched, and sequenced on Ion 530 Chip Ion Torrent S5 (Thermo
The aim to perform retrospective research using both whole Fisher Scientific, Waltham, MA, USA).
viral genome sequencing and molecular and epidemiological data
to understand the clusters of SARS-CoV-2 infection in Oman was to Genome assembly, annotation, and analysis
add context to the global data and international genomic
consortiums, and to give insight into the efficiency of the contact The Torrent Suite Software (version 12) (Thermo Fisher Scientific,
tracing system in the country. Waltham, MA, USA) with SARS-CoV-2 plugins (COVID19Annota-
teSnpEff, IRMAreport, and AssemblerTrinity) were installed and
Material and methods preoptimized with the reference sequence (ion_ampliseq_sars-
cov2) and target regions (Ion_Ampliseq_SARS-CoV-2.2020323.
Outbreak investigation and early transmission of SARS-CoV-2 in Oman Designed.bed) to trim, filter, quality check, assemble, and annotate
the samples. Additional built-in plugins such as coverage analysis
Data of laboratory-confirmed COVID-19 surveillance of Oman and variant caller were also used to understand the SNPs and
were included in this study from February 24 to May 23, 2020. mutations. Specifically, iterative refinement meta-assembler plu-
Samples were selected based on epidemiological characteristics that gins were used to identify low-frequency variants for highly variable
represent various cluster types (company versus family), geographi- RNA viruses as revealed by the manufacturer’s guidelines. To further
cal location, and nationality. The epidemiological investigation was validate, the obtained sequenced data were remapped with Wuhan-
conducted by public health teams throughout the country, who fed Hu-1 (GenBank accession number NC_045512.2).
data into a national electronic database. All confirmed cases
underwent epidemiological investigations and included the infor- Phylogenomic analysis
mation of each patient’s demography (age, gender, residency, and
nationality), epidemiology (source of infection if known, date of The sequence alignment and phylogenetic trees were generated
onset, primary case [infector] or secondary case [infected], and by following the Rob Lanfear’s method (Roblanf and Richard, 2020)
designation [cluster or sporadic]). The data were then analyzed to for a global phylogeny of SARS-CoV-2. All the sequences were
find out the relationship between the patients using the Epicontact R downloaded from GISAID websites and created a global sequence
library; further the description of the methods is found in a recent alignment. First, every sequence was aligned to the Wuhan
article by Al Wahaibi et al. (2020). reference genome (NC_045512.2) with the help of the script,
global_profile_alignment.sh, then joining the individually aligned
Specimen collection and inclusion criteria sequences into a global alignment at the end. To construct a
phylogenetic tree, the maximum likelihood (ML) method was used
Respiratory specimens collected from confirmed cases per the using the FastTree software (MicrobesOnline, Berkeley, CA, USA)
Ministry of Health national case definition were used in this study. with the best setting determined by GISAID. We further optimized
Samples were selected from main clusters since the start of local that tree with a series of minimum evolution SPR moves and ML
transmission for a period of two months, from March 23 to May 5, NNI moves in FastTree. The Letunic and Borks’ tool (2007) was used
2020. to visualize the trees. In the second phylogenetic analysis, 349
complete SARS-CoV-2 genome sequences (including 203 sequen-
RNA extraction, library preparation, and sequencing ces from Oman) were downloaded from GISAID. These sequences
were aligned to the Wuhan reference genome (NC_045512.2) using
A new method for SARS-CoV-2 sequencing by Thermo Fisher the above script. The above phylogenetic inference method was
Scientific was followed (Supplementary information 1). Briefly, the used to infer the tree as described above.
RNA extraction of samples was carried out through MagMaxTM
Viral Pathogen Extraction Kit (Thermo Fisher Scientific, Waltham, Results
MA, USA) or Viral RNA Isolation Kit with Liferiver EX3600 (Liferiver
Biotech, Hangzhou Bay, China), following manufacturer protocol. Epidemiology of SARS-CoV-2 infection in Oman
For the detection of the SARS-CoV-2 virus by real-time polymerase
chain reaction (RT-PCR) system, Novel Coronavirus (2019-nCoV) In this study, 21 clusters were identified with a total of 456
Nucleic Acid Diagnostic Kit, CE-IVD, FDA-EUA (Sansure Biotech, laboratory-confirmed cases of which 94 representative cases of

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different clusters with high viral load were selected for whole- transmission and trade. Cases selected from this cluster belonged
genome sequencing. Figure 1 describes selected clusters with their to B.1.1.27 (GR) genotype, and most of the clusters were distributed
month of transmission, genotype, geographical location, and type across different geographical locations because the origin of the
of cluster. Significant correspondence between the epidemiologi- cluster emerged from major cluster B extended to other locations.
cal and genetic data was observed. Five were major intrafamilial In addition, cluster P occurred in a company, and labor camps
clusters, three from the workplace, and two clusters were a belonged to clade B.1.127 (GR) genotype and spread the epidemic
mixture of both. The results also showed that the initial SARS-CoV- into four geographical locations (Muscat, Dakhiliyah, Al Batinah
2 infection cases were detected in March in the capital city of South, and Dhofar governorate). Family clusters have also
Muscat within a major trade and tourist destination (Mutrah) and contributed to the spread of the epidemic to the entire country,
were classified epidemiologically as cluster B (Figure 1). This as seen in cluster V, C, and I. As shown in Table 1, around 50% of the
cluster expanded during the months of April and May and spread cases were males, Omani nationals, and from Muscat governorate.
to North Sharqiyah and Dhahira as a result of community The majority (78.7%) were from the working age group, (15–50

Figure 1. Location of the governorates of the genotyped sample with the corresponding cumulative incidence of lab-confirmed COVID-19 per 100,000 population (part A),
and the weekly distribution of the genotyped sample with the total weekly confirmed cases (part B) in Oman from March 15 to May 23, 2020.

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Table 1 (GR) lineage within the E cluster of the Al Batinah South region
Descriptive statistics of the genotyped samples infected with SARS-CoV-2.
(EPI_ISL_491143 and EPI_ISL_491144) as shown in Figure 2.
Parameters Sample distribution (%)
Overall (N = 94) Phylogenomic analysis
Age group
0–14 Years 9 (9.6%) We performed a detailed phylogenomic analysis through ML of
15–50 Years 74 (78.7%)
the 94 sequenced samples. The whole viral genomes were aligned
>50 Years 11 (11.7%)
Gender
through a multiple alignment analysis and compared with the
MALE 54 (57.4%) Wuhan reference genome (Genbank: MN908947). The phyloge-
Nationality netic analysis was also supplemented with epidemiological
Omani 52 (55.3%) datasets of epi week of infection onset and distribution of the
Governorate
identified clusters across different geographical locations in Oman
Muscat 51 (54.3%)
Al Batinah South 23 (24.5%) (Figure 3). Generally, there was a good correlation between the
Dakhiliyah 9 (9.6%) epidemiologically defined clusters and their phylogenomic rela-
Dhahirah 8 (8.5%) tionship as shown with cluster B, V, I, G, R, X, and W. The
Buraimi 2 (2.1%)
phylogenetic tree in Figure 3 showed that cluster B started early,
North Sharqiyah 1 (1.1%)
Genotype
under a month following the first laboratory-confirmed cases
B (L) 1 (1.1%) identified in Oman. The outbreak continued for around six weeks.
B (O) 4 (4.3%) Sequences from this cluster belonged to B.1.1.27 (GR) and all were
B.1 (G) 3 (3.2%) closely related to each other except for one case lineage B (O) but
B.1.1 (GR) 18 (19.1%)
was found to be epidemiologically linked to the index case and was
B.1.1.27 (GR) 55 (58.5%)
B.1.1.27 (O) 2 (2.1%) within the same geographical location. It is also observed from
B.1.113 (GH) 10 (10.6%) Figure 4 that during weeks 16 and 17, multiple outbreaks were
B.6 (O) 1 (1.1%) detected that affected different geographical locations; clusters: B,
C, H, I, J, O, V, and W. The clusters were found to belong mostly to
B.1.1 lineage except for one cluster (V) that was B.1.36 (GH). Some
years). The results showed that the most frequent genotype was clusters were localized in specific governorates that shared a
B.1.1.27 (GR), 58.5%, followed by B.1.1 (GR), 19.1%. monophyletic clade within the phylogenetic tree such as cluster I,
which belonged to Dhahira and cluster V that was found in Al
Whole-genome sequencing of SARS-CoV-2 samples Batinah South having >90% bootstrap support.
To compare the distribution of SARS-CoV-2 sequences from
An amplicon-sequencing approach developed by Ion Torrent for Oman with other countries in the region and globally, we obtained
COVID-19 was adopted for the project that yielded a total of 13 Gb a subset of sequences from neighboring countries and cases with
of sequence data and over 56 million reads from 94 SARS-CoV-2 travel history within the same period of this study. In the second
samples (Supplementary Table S1). The genome coverage was phylogenetic tree (Figure 4), we analyzed 349 complete SARS-CoV-
99.8%, and the average genome size of SARS-CoV-2 was 29,834 bp 2 genomes sequences (including 203 sequences from Oman) that
(Supplementary Table S2). SARS-CoV-2 genome sequences gener- were downloaded from GISAIDS on September 1, 2020. The results
ated in this study have been deposited to GISAID.1 A list of all revealed that most sequences from Oman are closely related to
sequences with their accession numbers is provided in Supple- each other and shared the B.1.1 (GR) clade with related genomes
mentary Table S3. within the tree (Figure 4). Those sequences were closely related to
sequences from the United Arab Emirates, the Kingdom of Saudi
SARS-CoV-2 genomes from Oman Arabia, Kuwait, Bahrain, Bangladesh, Southeast Asia, and Europe.
Another clade, the B.1.36 (GH), was closely related to sequences
The results of whole-genome sequencing of SARS-CoV-2 obtained from KSA, Bahrain, Bangladesh, Iran, Tunisia, and UK.
revealed the presence of common mutations when compared Additionally, it was observed from the tree that Oman had
with the Wuhan reference sequence (hCoV-19/Wuhan/WIV04/ sequences from most of the identified clades or Pangolin lineages.
2019). In this study, around 66 variants were identified with (Figure 4).
variable frequencies and across different gene regions. The most
prevalent mutation was P323L (94.7%) found in the non-structural Discussion
protein 12 followed by the D614G (92.6%) in the Spike glycoprotein
(Supplementary Figure S1). Another mutation (G71S) in the To add context to the global data and international genomic
nonstructural protein 5 region was present at a frequency of consortiums, understand the spread of the virus, and support the
70% in the study sample (Supplementary Figure S1). Some of the epidemiological surveillance for pandemic management, in Oman
identified mutations were defining a specific clade such as G204R a sequencing initiative for SARS-CoV-2 was established. Herein, we
and D614G in the Spike protein that constitutes the B.1.1.27 and the describe the sequencing of genomes of 94 samples of SARS-CoV-2
B.1.1 (GR). Interestingly, the common G71S mutation was not seen selected based on epidemiological and laboratory characteristics,
in the family cluster I, which belonged to B.1.1 (GR). collected from initial cases from the early outbreak clusters
Two unique missense mutations were detected in this study; between March 22 and May 23, 2020. The consistency between the
I280V in the NSP15 and R502C in the NSP13, which existed at low epidemiological and genetic information highlights the effective-
frequencies of 6 (5.3%) and 2 (2.1%), respectively (Supplementary ness of epidemiological surveillance and outbreak investigations.
Figure S1). The mutation I280V belonged to lineage B.1.113 (GH), it The epidemiological data illustrate the extensive interaction
was detected in cluster V in Al Batinah South and Muscat. The between different types of clusters (company and family) and
second mutation was detected in two cases that belonged to B.1.1 the vast spread of the infection between other governorates in
Oman. This could be explained by the origin of the epidemic that
started from the main trade and tourist area in Muscat.
1
https://www.gisaid.org Furthermore, the spread of infections between governorates was

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Figure 2. Selected clusters with their month of transmission, genotype, geographical location, and type of cluster.

Figure 3. Phylogenetic trees were constructed for 94 SARS-CoV-2 complete genomes collected from Oman. The tree was constructed using the ML method. The numbers
above the branches are the bootstrap values for ML. Colored ranges represent epi weeks (from weeks 11 to 25). Stars and other ligands represent governorates of Oman, while
alphabetic letters denote different clusters in Oman.

propagated by the gatherings among extended Omani families as (Al-Mahruqi et al., unpublished data). The D614G was found to
well as in crowded labor camps, thereby resulting in infection be the second-highest mutation with a frequency of 92.6% (87/94)
among nonnationals. in our study. Sallam et al. (2020) showed that the D614G mutation
In this study, common and unique variants were identified from appeared to be taking over COVID-19 infections in the Middle East
the genomic analysis of SARS-CoV-2. The D614G mutation in the and North Africa (MENA) region as a significant increase in the
Spike protein has been reported in 116 countries mostly of B1 proportion was noticed from 63.0% in February 2020 to 98.5% in
lineages (GR, G, and GH clades). In Oman, it has been detected since June 2020 (p < 0.001). Two large phylogenetic clusters were
March 2020 among patients with travel history to Europe (UK, identified through the ML analysis, which showed the evidence of
Turkey, Spain, and Netherlands), India, Tanzania, and Qatar intercountry mixing of sequences dating back to February 8, 2020

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Figure 4. Phylogenetic trees constructed for 349 complete SARS-CoV-2 genome sequences (including 203 sequences from Oman) were downloaded from GISAID from March
to May 2020. The tree was constructed using the ML method. The numbers above the branches are the bootstrap values for ML. Colored ranges represent different countries.
Different color circles show different clades according to GISAID phylogeny.

and March 15, 2020. Another commonly observed mutation in this lineages in the country initially. This lined up with the multiple
study, P323L, was described as the most common in other introductions due to travel and before the travel restrictions on
countries; furthermore, the increasing ratio of P323L indicates March 29. Similar findings were observed in UAE (Tayoun et al.,
that this type of mutation may favor and enhance the transmission 2020; Alandijany et al., 2020). Early cases detected in Oman in
capacity of SARS-CoV-2 (Wang et al., 2020). Both D614G and P323L February 2020 with a travel history from Iran belonging to B.4 (O)
were prevalent and coexisted in this study with almost the same (Al-Mahruqi et al., unpublished data) were also closely related to
frequency. It was suggested that these coevolving mutations and cases from UAE, Lebanon, Bahrain, Pakistan, and Kuwait. However,
how they could impact viral fitness, breadth, and complexity of this clade was absent in the selected clusters of this study. Similar
clinical symptoms may be associated with new mutations and findings were observed from sequences in other clades, except for
adaptations (Kannan et al., 2020). According to GISAID, this G71S the dominant clade B.1.1 and B.1.1.27 lineage (GR clade) that caused
common mutation was first reported in February 2020 in Germany major outbreaks in the country. The B1.1 lineage (GR) comprising
(hCoV-19/Germany/BW-ChVir-1577/2020) and belongs to the B.1 both Spike D614G and nucleocapsid RG203KR mutations, was the
lineage (G and GR clades) (https://www.gisaid.org/, 6-11-2020). major clade found in Oman, which is inconsistent with the current
This mutation was reported in 26 countries, Oman had the second- globally predominant clade in Europe, Asia, South America, and
highest prevalence rate of 125/203 (61%) of the globally reported Africa.
cases (COVID-19 Genomics UK Consortium). In general, and according to data deposited to GISAID, countries
The unique mutation NSP15-I280V detected in this study is in tend to resemble the clades of their continents, with a few
the endoRNAse of the NSP15 genomic region of SARS-CoV-2. The exceptions. In China, the L clade (original) still dominates but other
I280V mutation has been reported in only three countries, Oman clades were obviously introduced after the reopening of the
was the first to report this mutation from a strain (hCoV-19/Oman/ country (Mercatelli and Giorgi, 2020).
11374/2020) collected on April 7, 2020 among the V cluster that Currently and globally, the predominant clade worldwide is G
was observed in Al Batinah South Governorate. The mutation was and its offspring GH and GR (74% of world sequenced genomes),
later reported in UK in a strain collected in April 2020, B.1. lineage which vary remarkably within continents, and this variation is well
(G), hCoV-19/England/CAMB-1AE373/2020 (CVR Bioinformatics, pronounced in Europe.
Glasgow, UK). Unfortunately, the origin of this mutation is not Interestingly, GH is most prevalent in USA while GR is dominant
known as no travel history could be linked to the index case of this in Europe and the most common worldwide. Regionally, in KSA, GH
cluster. This unique mutation is worth further investigation for its has the highest prevalence, which is possibly due to related travel
biological effect on the pathogenesis of the virus. It is of grave history with USA. Not unexpectedly, UAE has a blend of all clades,
importance to know the level of impact novel variants have on but GR is dominant. In contrast to KSA, GR is dominating in Oman,
disease severity (Hodcroft et al., 2020). which could be explained by related travel history with UK where
Phylogenetic analysis of all SARS-CoV-2 Oman sequences GR is prevalent (Mercatelli and Giorgi, 2020).
deposited in GISAID and compared with a subset of sequences According to GISAID, scarce published data are available on
obtained from other countries revealed the presence of several genetic characteristics of SARS-CoV-2 in the GCC region. Reviewing

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these sequences from KSA (419), UAE (148), Bahrain (27), Qatar admissions. However, with the excess sample selected, we
(16), Iran (18), and Kuwait (8) during the same period of our study managed to involve sufficient samples to cover adequate
revealed that GR clade was predominant in Oman and UAE, while epidemiological variations in our genotyped sample. This work
GH clade was dominant in KSA. However, the mutation G71S is needs to continue to get accumulated sequencing data and
only present in Oman. The genome sequencing of SARS-CoV-2 has genomic analysis across the spectrum of the cases in the country
proceeded worldwide at an extraordinary rate with numerous for understanding diversity, future mutation, and fine-tuning
published reports following the first published genome from primers used for the diagnosis based on local strains. The study
Wuhan. This fact, however, does not prove true in the MENA region confirms through genetic analysis the good quality of surveillance
where the literature in this area is scarce. It is noteworthy systems that prove to be robust during the early pandemic.
mentioning that there are a few reports from UAE (49 isolates),
Egypt (2 isolates), and Iran (7 isolates). However, in addition to the Conclusion
small number of samples used, these studies are based on the
phylogenetic analysis only and no association with epidemiologi- Oman’s robust surveillance system was very efficient in guiding
cal surveillance was performed (Tabibzadeh et al., 2020; Tayoun outbreak investigation processes in the country, and illustrates the
et al., 2020; Kandeil et al., 2020). future importance of molecular epidemiology in guiding the
From a timeline perspective, the current pandemic started with national response to outbreaks and pandemics. Our work adds
an original strain (L) then mutated in early 2020 to clade S and to a context to the global data and international genomic consortiums.
lesser extent, clade O. About two weeks later, clade V appeared that
mutated in NSP6 and ORF3a. Then clade G appeared at the end of Authors’ contributions
January 2020 and the first appearance of its subclades, GR and GH
(mutated in Spike D614G, ORF3a, and Q57H), emerged about three Samira Al-Mahruqi, Amina Al-Jardani, Hanan Al-Kindi, Samiha
weeks later (February 20, 2020). Since then, clade G and its Al-Kharusi, Intisar Al-Shukri and Aisha Al-Busaidi conducted the
derivatives have become the most dominant. lab work and wrote the draft of the manuscript. Adil Al Wahaibi
While infectiousness and transmissibility are closely related, conducted the epidemiological work and the sampling methodol-
they are not necessarily synonymous to one another, and therefore, ogy for the clusters and wrote the draft manuscript. Sajjad Asaf,
detailed studies are needed to decide whether or not the D614G Ahmed N. Al-Rawahi, Ahmed Al-Rawahi, Abdul Latif Khan, Majid
mutation has contributed to an increase in the number of Al-Salmani conducted the WGS, the bioinformatics work, and the
infections and not simply higher viral loads during infection (Volz writing of the draft of the manuscript. Ahmed Al-Harassi and Seif
et al., 2021 and COVID-19 Genomics UK Consortium, 2020a). Al-Abri supervised the study and participated in all stages of the
Interestingly the entire region is sharing the same common manuscript.
mutations within the same clades (COVID-19 Genomics UK
Consortium, 2020b). As the pandemic is ongoing, so is the likely Conflict of interest
rise to further mutations and possible exhibition of phenotypic
changes; our ability to assess and trace these variations will aid in The authors declare that they have no conflict of interest.
apt and timely response measures.
To the best of our knowledge, this is the first large-scale molecular Funding
epidemiology study of COVID-19 in the MENA region where the
whole-genome sequencing of 94 samples of SARS-CoV-2 was coupled The authors would like to thank the University of Nizwa for
with epidemiological surveillance of the early transmission of COVID- funding this project through its internal research grant (IG/01-20-
19 in Oman. This has allowed us to link the surveillance information UoN/01/NMSRC).
with the genetic analysis of the virus and enabled genotype tracking
and identifying the mutations present in circulating strains. In Ethical approval
addition, these results provide baseline information to which future
genomes can be compared to study evolution. The study was approved by the Directorate General for Disease
The main limitation of our study is that it is retrospective and Surveillance and Control, and there was no need for patients’
limited our ability in selecting certain epidemiological features for consent as the study was anonymous and used the data produced
the genotyped samples such as travel-related and severe for public health purposes.

Sr# Authors No of Country Originating Laboratory Accession ID

strains
1 Fatma 7 Turkey Ministry of Health Turkey EPI_ISL_428718, EPI_ISL_417413, EPI_ISL_428719,
Bayrakdar et al EPI_ISL_429862, EPI_ISL_429871, EPI_ISL_428723,
EPI_ISL_429864
2 Mehmet Turgut 1 Turkey
lık Bakanlıg
T.C. Sag _ Sag

ı Adıyaman Il
lık Müdürlüg

ü Adıyaman EPI_ISL_455719
et al.
itim Ve Araştırma Hastanesi
Eg
3 Ilker Karacan 1 Turkey enomic Laboratory (GLAB) (Conjoint lab of Health Directorate EPI_ISL_428368
et al of Istanbul and Istanbul Technical University)
4 Michael Carr 3 Ireland UCD National Virus Reference Laboratory EPI_ISL_418582, EPI_ISL_437684, EPI_ISL_500573
et al
5 Rodriguez,C 3 France Hôpital Henri-Mondor Ap-Hp EPI_ISL_447665, EPI_ISL_447658, EPI_ISL_447654
et al.
6 Mélanie Albert 2 France Sentinelles network EPI_ISL_421514, EPI_ISL_414600
et al
7 Antonin Bal et al 1 France Institut des Agents Infectieux (IAI), Hospices Civils de Lyon EPI_ISL_419178
8 Rasel Ahmed, 1 Bangladesh Bangladesh Institute of Tropical & Infectious Diseases, COVID- EPI_ISL_450339
Md et al 19 Testing Laboratory
9 3 Bangladesh National Institute of Laboratory Medicine and Referral Center EPI_ISL_504184, EPI_ISL_498816, EPI_ISL_466693

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(Continued)
Sr# Authors No of Country Originating Laboratory Accession ID
strains
Abu Sayeed
Mohammad
Mahmud et al
10 Md. Murshed 1 Bangladesh National Institute of Laboratory Medicine and Referral Center EPI_ISL_498800
Hasan Sarkar
et al
11 Senjuti Saha 1 Bangladesh Child Health Research Foundation EPI_ISL_477127
et al
12 Siyuan Yang et al 4 Beijing Laboratory of Infectious Diseases Center of Beijing Ditan EPI_ISL_452344, EPI_ISL_452333, EPI_ISL_452345,
Hospital EPI_ISL_455693
13 Lin Qi et al 1 Fujian Fujian Center for Disease Control and Prevention EPI_ISL_431783
14 Shengyue Wang 1 Shanghai Shanghai Public Health Clinical Center, Shanghai Medical EPI_ISL_416382
et al College, Fudan University
15 Gao,Q et al 2 Zhejiang Department of Microbiology EPI_ISL_455689, EPI_ISL_455688
16 Rita Feghali et al 2 Lebanon Rafik Hariri University Hospital EPI_ISL_450512, EPI_ISL_450511
17 Abi Habib,W 1 Lebanon Lebanese American University EPI_ISL_498551
et al
18 Issa Abu-Dayyeh 6 Jordan Biolab Diagnostic Laboratories EPI_ISL_429998, EPI_ISL_430011, EPI_ISL_429997,
et al EPI_ISL_450187, EPI_ISL_429994, EPI_ISL_429992
19 Mohd Noor Mat 2 Malaysia National Public Health Laboratory EPI_ISL_416885, EPI_ISL_528739
Isa et al
20 Yoong Min 3 Malaysia Department of Medical Microbiology, University Malaya EPI_ISL_501226, EPI_ISL_501206, EPI_ISL_501176
CHONG et al Medical Centre
21 Hajar Fauzan 1 Malaysia Microbiology Unit, Department of Pathology & Laboratory EPI_ISL_455313
Ahmad et al Medicine, IIUM Medical Centre
22 Suppiah J et al 1 Malaysia Institute for Medical Research, Infectious Disease Research EPI_ISL_490089
Centre, National Institutes of Health, Ministry of Health
Malaysia
23 Mak TM et al 12 Singapore National Public Health Laboratory, National Centre for EPI_ISL_462415, EPI_ISL_443231, EPI_ISL_462350,
Infectious Diseases EPI_ISL_428827, EPI_ISL_527370, EPI_ISL_462280,
EPI_ISL_443233, EPI_ISL_435698, EPI_ISL_443240,
EPI_ISL_462363, EPI_ISL_443223, EPI_ISL_475968
24 Danielle E 1 Singapore National Centre for Infectious Diseases EPI_ISL_420104
Anderson et al
25 Chen YYC et al 1 Singapore Department of Laboratory Medicine Tan Tock Seng Hospital EPI_ISL_492979
26 Pilailuk,Okada 3 Thailand Ramathibodi Hospital EPI_ISL_515468, EPI_ISL_447921, EPI_ISL_430842
et al
27 Elizabeth Batty 5 Thailand Ramathibodi Hospital EPI_ISL_429175, EPI_ISL_447011, EPI_ISL_512861,
et al EPI_ISL_458024, EPI_ISL_455915, EPI_ISL_455934
28 Rodpan,A et al 2 Thailand Faculty of Medicine EPI_ISL_437611, EPI_ISL_437624
29 Samira Al- 30 Oman Oman-NIC EPI_ISL_457701, EPI_ISL_457704, EPI_ISL_457706,
Maruqi et al EPI_ISL_457937, EPI_ISL_457938, EPI_ISL_457939,
EPI_ISL_457974, EPI_ISL_457975, EPI_ISL_457976,
EPI_ISL_457977, EPI_ISL_457978, EPI_ISL_457979,
EPI_ISL_457980, EPI_ISL_491116, EPI_ISL_457987,
EPI_ISL_457985, EPI_ISL_457986, EPI_ISL_457988,
EPI_ISL_457989, EPI_ISL_457990, EPI_ISL_457991,
EPI_ISL_457992, EPI_ISL_457993, EPI_ISL_457994,
EPI_ISL_457995, EPI_ISL_457996, EPI_ISL_457997,
EPI_ISL_457998, EPI_ISL_492065
30 Fahad Zadjali 68 Oman Oman-NIC EPI_ISL_457702, EPI_ISL_457703, EPI_ISL_457705,
et al EPI_ISL_457707, EPI_ISL_457981, EPI_ISL_457982,
EPI_ISL_457983, EPI_ISL_457984, EPI_ISL_458116,
EPI_ISL_458117, EPI_ISL_458118, EPI_ISL_458119,
EPI_ISL_458120, EPI_ISL_458121, EPI_ISL_458122,
EPI_ISL_458123, EPI_ISL_458124, EPI_ISL_458125,
EPI_ISL_458126, EPI_ISL_458127, EPI_ISL_458128,
EPI_ISL_458137, EPI_ISL_491968, EPI_ISL_491969,
EPI_ISL_491970, EPI_ISL_491971, EPI_ISL_491972,
EPI_ISL_491973, EPI_ISL_491974, EPI_ISL_491975,
EPI_ISL_491976, EPI_ISL_491977, EPI_ISL_491978,
EPI_ISL_491979, EPI_ISL_491980, EPI_ISL_491981,
EPI_ISL_491982, EPI_ISL_491983, EPI_ISL_491984,
EPI_ISL_491985, EPI_ISL_491986, EPI_ISL_491987,
EPI_ISL_491988, EPI_ISL_491989, EPI_ISL_491990,
EPI_ISL_491991, EPI_ISL_491992, EPI_ISL_491993,
EPI_ISL_491994, EPI_ISL_491995, EPI_ISL_491996,
EPI_ISL_491997, EPI_ISL_491998, EPI_ISL_491999,
EPI_ISL_492000, EPI_ISL_492001, EPI_ISL_492002,
EPI_ISL_492003, EPI_ISL_492004, EPI_ISL_492005,
EPI_ISL_492006, EPI_ISL_492007, EPI_ISL_492008,
EPI_ISL_492009, EPI_ISL_492010, EPI_ISL_492011,
EPI_ISL_492012, EPI_ISL_492013, EPI_ISL_492014,
EPI_ISL_492015, EPI_ISL_492016, EPI_ISL_492017,
EPI_ISL_492018, EPI_ISL_492019, EPI_ISL_492020,

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EPI_ISL_492021, EPI_ISL_492022, EPI_ISL_492023,

EPI_ISL_492024, EPI_ISL_492025, EPI_ISL_492026
31 Bas Oude 6 Bahrain Kingdom of Bahrein Ministry of Health EPI_ISL_483545, EPI_ISL_483546, EPI_ISL_483550,
Munnink et al EPI_ISL_483560, EPI_ISL_483561, EPI_ISL_483639,
32 Altaif,Z et al 1 Bahrain National Influenza Center, Bahrain EPI_ISL_486889
33 Zaed,A et al 1 Bahrain Communicable Disease Laboratory, Public Health Directorate EPI_ISL_487273
34 Al Wasti,H. and 1 Bahrain Communicable Disease Laboratory, Public Health Directorate EPI_ISL_510528
AlTaif,Z.
35 Shehab,F 1 Bahrain Communicable Disease Laboratory, Public Health Directorate EPI_ISL_510531
36 Zeinali,S et al 1 Iran Human Genetic Research Center, Kawsar Biotech Company EPI_ISL_424349
37 Shahabzadeh,Z 3 Iran Yaftabad Hospital, Covid Lab Center EPI_ISL_507007, EPI_ISL_514753, EPI_ISL_442044
38 Fahd Al-Mulla 4 Kuwait Dasman Diabetes Institute EPI_ISL_416543, EPI_ISL_421652, EPI_ISL_422426,
et al EPI_ISL_422427
39 Javed,A et al 1 Pakistan Department of Healthcare Biotechnology, National University EPI_ISL_417444
of Sciences and Technology (NUST)
40 Shakeel,M et al 1 Pakistan Jamil-ur-Rahman Center for Genome Research, Dr. Panjwani EPI_ISL_451958
Center for Molecular Medicine and Drug Research,
International Center for Chemical and Biological Sciences,
University of Karachi
41 Massab Umair 1 Pakistan Department of Virology, Public Health Laboratories Division, EPI_ISL_468163
et al National Institute of Health
42 Khan,M.T et al 1 Pakistan Microbiology & Bioinformatics and Biostatistics, Kohat EPI_ISL_513925
University of Science and Technology (Pakistan) & Shanghai
Jiao Tong University (China)
43 Sunil Raghav 2 India Institute of Life Sciences, Bhubaneswar EPI_ISL_463033, EPI_ISL_455761
et al
44 Pramod Kumar 3 India National Centre for Disease control (NCDC) EPI_ISL_436434, EPI_ISL_435111, EPI_ISL_435110
et al
45 Saurabh Kumar 1 India Translational Health Science and Technology Institute -ESIC EPI_ISL_528383
et al medical college and hospital, Faridabad
46 Dinesh Kumar 1 India GMERS Medical College and Hospital, Dharpur, Patan EPI_ISL_524758
et al
47 Arindam Maitra 1 India Indian Institute of Science EPI_ISL_508310
et al
48 Amit Kumar 2 Saudia Pathogen Genomics Lab King Abdullah University of Science EPI_ISL_513248, EPI_ISL_513241
Subudhi et al Arabia and Technology(KAUST)
49 Sharif Hala et al 2 Saudia Pathogen Genomics Lab King Abdullah University of Science EPI_ISL_437463, EPI_ISL_437756
Arabia and Technology(KAUST)
50 Majed Alghoribi 1 Saudia Clinical Microbiology Lab EPI_ISL_416432
et al Arabia
51 Sara Mfarrej 1 Saudia Pathogen Genomics Lab King Abdullah University of Science EPI_ISL_512978
et al Arabia and Technology(KAUST)
52 Afrah Alsomali 1 Saudia Pathogen Genomics Lab King Abdullah University of Science EPI_ISL_513257
et al Arabia and Technology(KAUST)
53 Ahmad Abou 6 UAE Mohammed Bin Rashid University of Medicine and Health EPI_ISL_520695, EPI_ISL_463740, EPI_ISL_520718,
Tayoun et al Sciences EPI_ISL_520681, EPI_ISL_520708, EPI_ISL_520738
54 Ortwin Adams 2 Germany Center of Medical Microbiology, Virology, and Hospital EPI_ISL_425123, EPI_ISL_425130
et al Hygiene, University of Duesseldorf
55 Max 3 Germany Max von Pettenkofer Institute, Virology, National Reference EPI_ISL_466905, EPI_ISL_451940, EPI_ISL_437284
Muenchhoff Center for Retroviruses, LMU München
et al
56 Peter Bauer and 2 Germany Centogene AG EPI_ISL_459964, EPI_ISL_459962
Krishna Kumar
Kandaswamy
57 Lorusso A et al 1 Italy Ospedale "Ss. Annunziata" EPI_ISL_529014
58 Antonio Mori 1 Italy IRCCS Sacro Cuore Don Calabria Hospital, Department of EPI_ISL_492985
et al Infectious, Tropical Diseases & Microbiology
59 Paola Stefanelli 1 Italy Department of Infectious Diseases, Istituto Superiore di Sanità, EPI_ISL_412974
et al Rome, Italy
60 Guillermo 1 Spain Servicio de Microbiología y Parasitología clínica. UCEIMP. EPI_ISL_452570
Martín Hospital Universitario Virgen del Rocío/IBIS/CSIC/US.
Gutiérrez et al
61 Salud 2 Spain Hospital Universitario Puerta del Mar de Cádiz - INIBICA EPI_ISL_467071, EPI_ISL_467080
Rodríguez-
Pallares, et al
62 Gustavo Cilla 1 Spain Servicio de Microbiología. Hospital Universitario Donostia. OSI EPI_ISL_452688
et al Donostialdea. Área de Enfermedades Infecciosas, Grupo
63 Antonio Rezusta 1 Spain Servicio de Microbiología, Hospital Miguel Servet, Zaragoza EPI_ISL_468780
López et al
64 McHugh M 1 Schotland Virology Department, Royal Infirmary of Edinburgh, NHS EPI_ISL_426007
Lothian / School of Biological Sciences, University of Edinburgh
/ Institute of Genetics and Molecular Medicine, University of
Edinburgh
65 Sam Haldenby 1 England Liverpool Clinical Laboratories EPI_ISL_517180
et al
66 Luke W 3 England Department of Pathology, University of Cambridge EPI_ISL_441294, EPI_ISL_442841, EPI_ISL_441294
Meredith et al
67 Claire 2 England University of Birmingham EPI_ISL_529403, EPI_ISL_529603
McMurray et al
68 1 England EPI_ISL_421780

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(Continued)
Sr# Authors No of Country Originating Laboratory Accession ID
strains
Monica Galiano Respiratory Virus Unit, Microbiology Services Colindale, Public
et al Health England
69 PHE Covid 1 England Respiratory Virus Unit, Microbiology Services Colindale, Public EPI_ISL_464480
Sequencing Health England
Team
70 Ling Li, et al 1 England North West London Pathology, Imperial College Healthcare EPI_ISL_524656
NHS Trust
71 Tracy Basler et al 1 USA San Diego County Public Health Laboratory EPI_ISL_467956
72 Gage Moreno 1 USA University of Wisconsin-Madison AIDS Vaccine Research EPI_ISL_417200
et al Laboratories
73 CZB Cliahub 1 USA Humboldt County Public Health Laboratory EPI_ISL_454639
Consortium
74 Lemieux,J.E et al 1 USA Massachusetts General Hospital EPI_ISL_460422
75 Michael Quigley 1 USA Scripps Medical Laboratory EPI_ISL_437582
et al
76 Anna Uehara 1 USA Pathogen Discovery, Respiratory Viruses Branch, Division of EPI_ISL_413609
et al Viral Diseases, Centers for Dieases Control and Prevention
77 Matt Plumb et al 1 USA Minnesota Department of Health, Public Health Laboratory EPI_ISL_482949
78 Matluk,N et al 1 USA Maine HETL EPI_ISL_513470
79 CZB Cliahub 3 USA County of Santa Clara Public Health EPI_ISL_437061, EPI_ISL_436679, EPI_ISL_468445
Consortium
80 Chu et al 1 USA Washington State Department of Health EPI_ISL_463547
81 Chen J et al 1 USA Alaska State Virology Laboratory EPI_ISL_512151
82 Fares,W. and 3 Tunisia Clinical virology EPI_ISL_463002, EPI_ISL_463003, EPI_ISL_463005
Triki,H.
83 Handrick,S et al 1 Tunisia Bundeswehr Institute of Microbiology EPI_ISL_458286
84 Mohamed 1 Egypt Center of Scientific Excellence for Influenza Viruses,National EPI_ISL_430819
Ahmed Ali et al Research Centre (NRC), Egypt.
85 Zekri, Abdel 2 Egypt Egyptian National Cancer Institute (ENCI) EPI_ISL_468045, EPI_ISL_468062
Rahman et al

Acknowledgments Grubaugh ND, Ladner JT, Lemey P, Pybus OG, Rambaut A, Holmes EC, et al. Tracking
virus outbreaks in the twenty-first century. Nat Microbiol 2019;4(1):10–9, doi:
http://dx.doi.org/10.1038/s41564-018-0296-2.
We would like to thank Dr Saqib Bilal and Mr Adil Khan for their Hill V, Rambaut A. Phylodynamic analysis of SARS-CoV-2, Update 20320-03-06.
experimental help in library preparation and sequencing. We also 2020. . [Accessed 13 November 2020] https://virological.org/t/phylodynamic-
would like to thank Mr Ali Al-Abri for preparing the graphs and analysis-of-sars-cov-2-update-2020-03-06/420.
Hodcroft EB, Zuber M, Nadeau S, Comas I, Candelas FG, SeqCOVID-SPAIN
tables. We express our gratitude to the collective endeavor of the consortium, et al. Emergence and spread of a SARS-CoV-2 variant through
GISAID consortium and to the thousands of contributing laborato- Europe in the summer of 2020. medRxiv Preprint 2020;, doi:http://dx.doi.org/
ries that made comparative genomics possible. We would like to 10.1101/2020.10.25.20219063 https://www.gisaid.org/ [6-11-2020].
Kandeil A, Mostafa A, El-Shesheny R, Shehata M, Roshdy WH, Ahmed SS, et al.
thank the Oman Animal and Plant Genetic Resource Center Coding complete genome sequences of two SARSCoV-2 isolates from Egypt.
(OAPGRC) for their support of NGS. We also acknowledge Lesley Microbiol Resour Announc 2020;9:e00489–20, doi:http://dx.doi.org/10.1128/
Carson for her help in the English editing and proofreading of the MRA.00489-20.
Kannan SR, Spratt AN, Quinn TP, et al. Infectivity of SARS-CoV-2: there is something
manuscript.
more than D614G?. J Neuroimmune Pharmacol 2020;1–4, doi:http://dx.doi.org/
10.1007/s11481-020-09954-3.
Appendix A. Supplementary data Khan JS, McIntosh K. History and recent advances in coronavirus discovery. Pediatr
Infect Dis J 2005;24(11):S223–227, doi:http://dx.doi.org/10.1097/01.
inf.0000188166.17324.60.
Supplementary material related to this article can be found, in the Letunic I, Bork P. Interactive Tree of Life (iTOL): an online tool for phylogenetic tree
online version, at doi:https://doi.org/10.1016/j.ijid.2020.12.049. display and annotation. Bioinformatics 2007;23(1):127–8, doi:http://dx.doi.
org/10.1093/bioinformatics/btl529.
Mercatelli D, Giorgi FM. Geographic and genomic distribution of SARS-CoV-2
References mutations. Front Microbiol 2020;11:1800, doi:http://dx.doi.org/10.3389/
fmicb.2020.01800.
Al Wahaibi A, Al Manji A, Al Maani A, Al Rawahi B, Al Harthy K, Alyaquobi F, et al. Ministry of Health, Oman. www.moh.gov.om more than 115,000 infected cases and
COVID-19 epidemic monitoring after non-pharmaceutical interventions: the about 1200 death PLEASE FIND Title. DIRECT LINK. 2020 [Accessed XX
use of time-varying reproduction number in a country with a large migrant November 2020].
population. Int J Infect Dis 2020;99:466–72, doi:http://dx.doi.org/10.1016/j. Minskaia E, Hertzig T, Gorbalenya AE, Campanacci V, Cambillau C, Canard B, et al.
ijid.2020.08.039. Discovery of an RNA virus 30 →50 exoribonuclease that is critically involved in
Alandijany TA, Faizo AA, Azhar EI. Coronavirus disease of 2019 (COVID-19) in the coronavirus RNA synthesis. Proc Natl Acad Sci U S A 2006;103(13):5108–13, doi:
Gulf Cooperation Council (GCC) countries: current status and management http://dx.doi.org/10.1073/pnas.0508200103.
practices. J Infect Public Health 2020;13(6):839–42, doi:http://dx.doi.org/ Paules CI, Marston HD, Fauci AS. Coronavirus infections—more than just the
10.1016/j.jiph.2020.05.020. common cold. JAMA 2020;323(8):707–8, doi:http://dx.doi.org/10.1001/
Al-Mahruqi, et al., unpublished data. jama.2020.075.
COVID-19 Genomics UK Consortium. CoV-GLUE enabled by data from GISAID. 2020. Roblanf, Richard M. A global phylogeny of SARS-CoV-2 sequences from GISAID.
. [Accessed 13 November 2020] http://cov-glue.cvr.gla.ac.uk/. Zenodo 2020;, doi:http://dx.doi.org/10.5281/zenodo.4051213 In preparation.
COVID-19 Genomics UK Consortium. Report #9-25th June 2020. 2020. . https:// Sallam M, Ababneh N, Dababseh D, Bakri F, Mahafz A. Temporal increase in D614G
www.gisaid.org/. [6-11-2020] https://www.cogconsortium.uk/wp-content/ mutation of SARS-CoV-2 in the Middle East and North Africa: phylogenetic and
uploads/2020/07/2. mutation analysis study. medRxiv Preprint 2020;, doi:http://dx.doi.org/10.1101/
Fehr AR, Perlman S. Coronaviruses: an overview of their replication and 2020.08.24.20176792 Submitted for publication.
pathogenesis. In: Maier HJ, Bickerton E, Britton P, editors. Coronaviruses: Tabibzadeh A, Zamani F, Laali A, Esghaei M, Tameshkel F, Keyvani H, et al. SARS-CoV-
methods and protocols. New York: Springer; 2015. p. 1–23. 2 molecular and phylogenetic analysis in COVID-19 patients: a preliminary
GISAID. GISAID_hCoV-19_Analysis_Update_2020-10-23_1500UTC.pdf. 2020. . [Accessed 13 report from Iran. Infect Genet Evol 2020;84:104387, doi:http://dx.doi.org/
November 2020] https://www.yunzhan365.com/basic/92100557.html. 10.1016/j.meegid.2020.104387.

148
S. Al-Mahruqi, A. Al-Wahaibi, A.L. Khan et al. International Journal of Infectious Diseases 104 (2021) 139–149

Tayoun AA, Loney T, Khansaheb H, Ramaswamy S, Harilal D, Deesi ZO, et al. Wang R, Chen J, Gao K, Hozumi Y, Yin C, Wei GW. Characterizing SARS-CoV-2
Multiple early introductions of SARS-CoV-2 into a global travel hub in the mutations in the United States, Version 1. Res Sq Preprint 2020;(August), doi:
Middle East. Sci Rep 2020;10:17720, doi:http://dx.doi.org/10.1038/s41598- http://dx.doi.org/10.21203/rs.3.rs-49671/v1.
020-74666-w. WHO. WHO coronavirus disease (COVID-19) dashboard. 2020. . [Accessed 9
Volz E, Hill V, McCrone JT, Price A, Jorgensen D, O’Toole A, et al. Evaluating the effects December 2020] https://covid19.who.int/.
of SARS-CoV-2 Spike mutation D614G on transmissibility and pathogenicity. Wu A, Peng Y, Huang B, Ding X, Wang X, Niu P, et al. Genome composition and
Cell 2021;184(1)64–75, doi:http://dx.doi.org/10.1016/j.cell.2020.11.020 In this divergence of the novel coronavirus (2019-nCoV) originating in China. Cell Host
issue. Microbe 2020;27(3):325–8, doi:http://dx.doi.org/10.1016/j.chom.2020.02.001.

149