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A Comprehensive Molecular Epidemiological Analysis Of viruses Article A Comprehensive Molecular Epidemiological Analysis of SARS-CoV-2 Infection in Cyprus from April 2020 to January 2021: Evidence of a Highly Polyphyletic and Evolving Epidemic Andreas C. Chrysostomou 1, Bram Vrancken 2 , George Koumbaris 3, George Themistokleous 4, Antonia Aristokleous 1, Christina Masia 4, Christina Eleftheriou 5, Costakis Ioannou 4, Dora C. Stylianou 1, Marios Ioannides 3, Panagiotis Petrou 4 , Vasilis Georgiou 1 , Amalia Hatziyianni 4, Philippe Lemey 2, Anne-Mieke Vandamme 2,6 , Philippos P. Patsalis 3,7 and Leondios G. Kostrikis 1,* 1 Department of Biological Sciences, University of Cyprus, Aglantzia, Nicosia 2109, Cyprus; [email protected] (A.C.C.); [email protected] (A.A.); [email protected] (D.C.S.); [email protected] (V.G.) 2 Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, 3000 Leuven, Belgium; [email protected] (B.V.); [email protected] (P.L.); [email protected] (A.-M.V.) 3 NIPD Genetics Limited, Nicosia 2409, Cyprus; [email protected] (G.K.); [email protected] (M.I.); [email protected] (P.P.P.) 4 Medical Laboratory of Ammochostos General Hospital, Ammochostos General Hospital, Citation: Chrysostomou, A.C.; Paralimni 5386, Cyprus; [email protected] (G.T.); [email protected] (C.M.); Vrancken, B.; Koumbaris, G.; [email protected] (C.I.); [email protected] (P.P.); [email protected] (A.H.) 5 Themistokleous, G.; Aristokleous, A.; Department of Health and Safety, University of Cyprus, Aglantzia, Nicosia 2109, Cyprus; [email protected] 6 Masia, C.; Eleftheriou, C.; Ioannou, C.; Center for Global Health and Tropical Medicine, Unidade de Microbiologia, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, 1349-008 Lisbon, Portugal Stylianou, D.C.; Ioannides, M.; et al. 7 Medical School, University of Nicosia, Nicosia 2417, Cyprus A Comprehensive Molecular * Correspondence: [email protected]; Tel.: +357-2-289-2885 Epidemiological Analysis of SARS-CoV-2 Infection in Cyprus from Abstract: The spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) resulted in April 2020 to January 2021: Evidence of a Highly Polyphyletic and an extraordinary global public health crisis. In early 2020, Cyprus, among other European countries, Evolving Epidemic. Viruses 2021, 13, was affected by the SARS-CoV-2 epidemic and adopted lockdown measures in March 2020 to limit the 1098. https://doi.org/10.3390/ initial outbreak on the island. In this study, we performed a comprehensive retrospective molecular v13061098 epidemiological analysis (genetic, phylogenetic, phylodynamic and phylogeographic analyses) of SARS-CoV-2 isolates in Cyprus from April 2020 to January 2021, covering the first ten months of Academic Editor: Vittorio Sambri the SARS-CoV-2 infection epidemic on the island. The primary aim of this study was to assess the transmissibility of SARS-CoV-2 lineages in Cyprus. Whole SARS-CoV-2 genomic sequences Received: 6 May 2021 were generated from 596 clinical samples (nasopharyngeal swabs) obtained from community-based Accepted: 4 June 2021 diagnostic testing centers and hospitalized patients. The phylogenetic analyses revealed a total of Published: 9 June 2021 34 different lineages in Cyprus, with B.1.258, B.1.1.29, B.1.177, B.1.2, B.1 and B.1.1.7 (designated a Variant of Concern 202012/01, VOC) being the most prevalent lineages on the island during the Publisher’s Note: MDPI stays neutral study period. Phylodynamic analysis showed a highly dynamic epidemic of SARS-CoV-2 infection, with regard to jurisdictional claims in with three consecutive surges characterized by specific lineages (B.1.1.29 from April to June 2020; published maps and institutional affil- iations. B.1.258 from September 2020 to January 2021; and B.1.1.7 from December 2020 to January 2021). Genetic analysis of whole SARS-CoV-2 genomic sequences of the aforementioned lineages revealed the presence of mutations within the S protein (L18F, DH69/V70, S898F, DY144, S162G, A222V, N439K, N501Y, A570D, D614G, P681H, S982A and D1118H) that confer higher transmissibility and/or antibody escape (immune evasion) upon the virus. Phylogeographic analysis indicated Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. that the majority of imports and exports were to and from the United Kingdom (UK), although This article is an open access article many other regions/countries were identified (southeastern Asia, southern Europe, eastern Europe, distributed under the terms and Germany, Italy, Brazil, Chile, the USA, Denmark, the Czech Republic, Slovenia, Finland, Switzerland conditions of the Creative Commons and Pakistan). Taken together, these findings demonstrate that the SARS-CoV-2 infection epidemic in Attribution (CC BY) license (https:// Cyprus is being maintained by a continuous influx of lineages from many countries, resulting in the creativecommons.org/licenses/by/ establishment of an ever-evolving and polyphyletic virus on the island. 4.0/). Viruses 2021, 13, 1098. https://doi.org/10.3390/v13061098 https://www.mdpi.com/journal/viruses Viruses 2021, 13, 1098 2 of 30 Keywords: SARS-CoV-2; Covid-19; Cyprus; molecular epidemiology 1. Introduction Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was discovered in December 2019 in Wuhan City, China (the capital of Hubei Province), and since then, has caused a pandemic [1]. The virus spread rapidly with unprecedented infectivity, especially in comparison to previous coronavirus epidemics, such as the severe acute respiratory syn- drome (SARS) coronavirus (SARS-CoV) [2] and Middle East respiratory syndrome (MERS) epidemics [3]. This is evident from the fact that shortly after the start of the pandemic in January 2020, there were as many as 9927 cumulative cases of SARS-CoV-2 infections detected in at least 23 different countries/regions [4,5], and by the first quarter of 2021, there were more than 116,879,152 cases in 192 different countries/regions [4,5]. Significant factors that influenced the viral spread were the lack of herd immunity since methods such as vaccination against SARS-CoV-2 and effective pharmaceutical treatment/cure options had not yet been developed [6,7]. Thus, countries/regions opted to rely on policies such as social distancing, work closures, curfews, quarantine, travel and shopping restrictions to protect the population and prevent the collapse of health and economic systems [8,9]. These policies were implemented in conjunction with mass monitoring/screening of populations and contact tracing for SARS-CoV-2-positive individuals. However, such systems still place a heavy burden on the economy and are not permanent solutions [6]. Effective treatment and immunization methods are lacking [6,7], and disease prevention policies are mostly reactive to increases in SARS-CoV-2 cases, which facilitates a decrease in cases but does not prevent the spread of the virus. Thus, until the population is immunized and effective treatment is developed, it is important to optimize the current measures and policies [10]. This can be achieved by utilizing viral samples obtained from population monitor- ing and screening programs implemented by the government for the identification of SARS-CoV-2-infected individuals; analyzing and sequencing such samples provides the necessary basis for molecular epidemiological studies [11]. Molecular epidemiology has already provided significant insights into the evolution of this virus, and is currently being used to monitor/detect the accumulation of mutations in the viral genome [10,12]. It is important to note that SARS-CoV-2 is an RNA virus with proof-reading capabilities; how- ever, it is evident that this is not enough to prevent the accumulation of mutations [13,14]. Furthermore, this virus has a global distribution, infecting populations of different genetic backgrounds, ages and health statuses, and it is subjected to evolutionary and selection pressures imposed by the host’s immune system, as well as by antiviral drugs [13,15,16]. Consequently, this results in the generation of viral lineages with slightly altered genetic make-ups and novel viral diversity in need of classification [17]. Although the SARS-CoV- 2 nomenclature system has yet to be fully recognized, this study uses the viral lineage classification described by Rambaut et al. [17], who employed a phylogenetic framework to identify the lineages that contribute most to active spread [4,17,18]. Such classification systems are necessary for molecular epidemiological studies, since they enable the charac- terization of SARS-CoV-2 found in different population groups and niches, its diaspora, and its temporal dynamics and origins [19]. By identifying lineages varying in phenotype or antigenicity, health officials can remain alert and adequately prepare to safeguard public health [20]. Thus far, the evolution of SARS-CoV-2 has been continuously documented, with the S and L variants being reported at the end of February 2020 [21]; since then, its genetic variability has continued to expand. By March 2020, the D614G substitution, along with other accompanying mutations, started to sporadically appear, and by June 2020, it was prevalent enough to be present in over 74% of all published sequences [22]. Currently, there is a plethora of lineages with accumulated mutations circulating worldwide. In countries such as the UK, where the genetic diversity of the virus has been extensively described,
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