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. 2023 Nov 6;339:199259. doi: 10.1016/j.virusres.2023.199259

Detection of a cluster of Omicron's BA.4 sublineage in Northern Senegal and identification of the first XAS recombinant variant in Senegal

Martin Faye a,1,⁎, Modeste Name Faye a,1, Babacar Ndiaye b, Moussa Moïse Diagne a, Safietou Sankhe a, Ndeye Marième Top c, Amadou Diallo c, Cheikh Loucoubar c, Ndongo Dia a, Amadou Alpha Sall a, Ousmane Faye a
PMCID: PMC10652113  PMID: 37926155

Highlights

  • •

    Identification of the first recombinant XAS sequence reported from Senegal.

  • •

    Characterization of the origin of cluster of infections with the BA.4 sublineage.

  • •

    Rapid expansion and sustained local transmission of the BA.4 sublineage in Senegal.

Keywords: SARS-CoV-2 genomic surveillance, Omicron BA.4, First XAS recombinant, Senegal

Abstract

In Senegal, since its first detection in early March 2020, genomic surveillance of SARS-CoV-2 isolates has led to the identification of the emergence of the Omicron BA.4 and BA.5 sublineages from early June 2022. To investigate the origin of a cluster of cases in Northern Senegal on July 2022, isolates were analysed using Next-generation sequencing and phylogeny.

Our data provided evidence of the origin of the cluster of BA.4 cases from a XAS recombinant, that is to date, the first reported sequence of this variant from Senegal. Continuous genomic surveillance of positive SARS-CoV-2 samples is a crucial need.

1. Background

Since the end of December 2019, the world has been facing a COVID-19 pandemic with the Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) belonging to the Coronaviridae family as responsible agent. As of August 30th, 2023, a total of 770.085.713 confirmed cases of COVID-19, including more than 6 million deaths, has been reported to the World Health Organization (WHO) (WHO, 2023).

The dynamics of the COVID-19 pandemic have been much driven by the appearance of variants of interest (Soriano et al., 2022). Indeed, continuous evolution of the SARS-CoV-2 virus led to the consecutive emergence of several lineages ranging from the Alpha lineage to the most recent Omicron lineage (B.1.1.529) (Chouikha et al., 2022). First identified in Botswana and South-Africa in November 2021, the Omicron lineage was associated with a high transmissibility (Araf et al., 2022) and, a rapid global dispersal (Chouikha et al., 2022) which led to its rapid differentiation in sublineages (BA.1 to BA.5) and descendent recombinant lineages (XA to XW) (Tegally et al., 2022). Previous studies have shown the evident impact of clusters of cases in the super-spread of the SARS-COV-2 (Jeon et al., 2023; Alsayyad et al., 2023).

These recombination phenomena occur when two lineages co-infect the same cell of an individual (Jackson et al., 2021). There is thus a strong chance, during the replication of the genome, that the polymerase passes from a genomic sequence model to the heterologous genome. This then results in a recombinant virus in which part of its genome comes from one “parent” and the rest of the genomic sequence from the other (Carabelli et al., 2023).

In Senegal, the first confirmed COVID-19 case was identified on March 2, 2020 (Dia et al., 2020) and 89,014 confirmed cases including 1971 deaths have been recorded as of August 30th, 2023 (WHO, 2023). Despite the implementation of important public health countermeasures by the Senegalese Ministry of Health (MoH) (Dia et al., 2020; Diarra et al., 2022), four major epidemic waves followed by a short epidemic peak were previously recorded in the country from May 2020 to July 2022 (Diagne et al., 2022). Recorded between November 2021 and February 2022, the 4th wave involved the BA.1 and BA.2 sublineages whilst the following peak of confirmed cases from mid-June to July 2022 was related to the emergence of the BA.4 and BA.5 sublineages in Senegal and the co-circulation with some other Omicron recombinants (Diagne et al., 2022).

On July 05, 2022, a 36 years-old asymptomatic woman, resident of the Saint-Louis medical region (Northern Senegal), tested positive for SARS-CoV-2 during her COVID-19 testing for the 2022 pilgrimage at the Mecca (Saudi Arabia). The case was confirmed at the Institut Pasteur de Dakar's (IPD) campus in Dakar (Western Senegal), designated as one of the reference labs in Senegal in charge of COVID-19 testing for outbound travellers according to the regulations in force for all incoming and outgoing travellers (www.flyairsenegal.com) (Fig. S1). Epidemiological investigations around the case within the 48 h, helped identify that she received a second dose of the Pfizer-BioNTech COVID-19 vaccine four days ago and revealed no history of travel or participation to mass-gathering during the last 14 days preceding her testing. In addition, clinical specimens of nasopharyngeal swab from 10 out of 16 close contacts (including her husband) tested positive for SARS-CoV-2 at the IPD's mobile lab deployed in the Saint-Louis region through the national program for decentralized diagnosis of COVID-19 in Senegal (Fig. S1).

Herein, we reported on the origin of a cluster of COVID-19 infections in the Saint-Louis medical region using serological and molecular testing, next-generation sequencing (NGS) and phylogenetic analyses of the newly generated SARS-CoV-2 sequences.

2. Methods

From July 07 to July 13, 2022, the evolution of viral load was monitored for the 36 years-old woman (YB) and her 42 years-old husband (ON) during follow-up at their home. Nasopharyngeal swabs were collected every two days and tested by reverse-transcriptase and quantitative polymerase chain reaction (RT-qPCR) until obtaining a negative result. Sera were collected from the two cases on July 9 and 11, 2022 for detection of specific antibodies to SARS-CoV-2 using the NowCheck™ COVID-19 IgM/IgG rapid diagnostic test (RDT) (BioNote, Korea). In addition, the levels of SARS-CoV-2 specific anti-Spike protein immunoglobulin G (IgG) were assessed using Enzyme-linked Immunosorbent assay (ELISA) as previously described (Vigan-Womas et al., 2023).

On July 13, 2022, nasopharyngeal swabs were also collected from fifteen other suspected close contacts sharing the same household and who started developing COVID-19 symptoms and tested by RT-qPCR at the IPD's mobile lab in Saint-Louis using the nCoV-Qs kit (MiCo BioMed Co., Ltd. Republic of Korea) according to the manufacturer's instructions.

Demographic, clinical and exposure history information were collected from all sampled people. Positive specimens were sequenced by NGS on an Illumina MiSeq equipment and consensus sequences were generated as previously described (Diagne et al., 2022) and submitted in GISAID.

The generated sequences were first manually curated. Multiple alignments with SARS-CoV-2 sequences previously available in GISAID was performed using the FFT-NS-i method implemented in the MAFFT program (version 7.511) (Tabei et al., 2008). Potential recombination events were assessed using our sequence dataset with the RDP4 (Recombination Detection Program version 4) program (Martin et al., 2015), considering an event as significant if it was confirmed by at least 5 of the 7 selected methods using default settings, including RDP, GENECONV, Maxchi, Bootscan, Siscan, Chimaera, 3Seq and LARD. The Maximum-Likelihood (ML) phylogenetic tree was inferred using the IQ-Tree software (Nguyen et al., 2015) for 10,000 replications and the topology was visualized using the Figtree software (version v1.4.4).

3. Results

3.1. Assessment of serological markers

Serological testing of sera from the 36 years-old woman (YB) and her husband (ON) on July 9 and 11, 2022, showed the presence of anti-SARS-CoV-2 IgG while the specimens tested negative for anti-SARS-CoV-2 IgM. Assessment of the anti-SARS-CoV-2 IgG levels at two days interval exhibited a significant increase of IgG for both cases (2-log) between July 9 and July 11, 2022. Although the viral load fluctuated and showed no significant decrease from July 9 to 11, 2022 (Ct values ranging between 21.33 and 32.82), both cases tested negative for SARS-CoV-2 RNA on July 13, 2022 (Table 1).

Table 1.

Assessment and monitoring of viral load and specific antibodies to SARS-CoV-2 levels for the two first confirmed cases.

Date of testing YB
 ON
Sequencing ID1 ΔOD2 value from IgG3 ELISA Ct values Sequencing ID1 ΔOD2 value from IgG3 ELISA Ct value4
07/05/2022 YB0 Not done 27 Not done Not done Not done
07/07/2022 YB1 Not done 21.33 ON1 Not done 29.1
07/09/2022 YB2 1.840 32.82 ON2 1.086 29.73
07/11/2022 YB3 (505,691_SL) 3.435 31.10 ON3 (505,690_SL) 2.542 27.33
07/13/2022 YB4 Not done Negative ON4 Not done Negative
Open in a new tab

YB and ON reported no symptoms throughout follow-up and no prior SARS-CoV-2 infection was notified.

1

Identification number.

2

Difference in Optical density between the sample and the negative control.

3

Immunoglobulin G.

4

Threshold cycle value.

3.2. Presentation of the contacts

The other patients sampled (n = 15) had a median age of 28.7 years old (ranging 9–80 years) with 9 women and 6 men. The two main symptoms identified in this group included cough (100%) and sore throat (67%). An overall rate of 60% of these contacts (n = 9) tested positive for SARS-CoV-2 RNA with Ct values ranging between 14.19 and 31.09 (Table S1).

3.3. Recombination analysis and phylogeny

Significant recombination events were only found for two newly characterized isolates, exhibiting breakpoints at nucleotide positions 128 and 21,548 for sequence 505,699_SL and a breakpoint at nucleotide position 15,468 for 505,707_SL. In fact, the genomic region between nucleotide positions 192–21,546 and 1–15,468 on sequence of isolates 505,699_SL and 505,707_SL, displayed a relatively high degree of similarity to the 505,712_SL sequence from Senegal (Fig. S2). Complete genome sequences were obtained from 11 SARS-CoV-2 positive samples including those from YB, ON and the 9 close contacts, as previously described (Diagne et al., 2022). The ML tree showed that 90% (n = 10) of the newly characterized sequences belonged to the BA.4 sublineage while one isolate clustered with sequences belonging to the XAS recombinant sublineage (n = 1). All BA.4 sequences (n = 10) from Saint-Louis grouped in a unique sub-clade and were related to previous Senegalese isolates identified in June 2022, suggesting a rapid expansion and a sustained local transmission of the BA.4 sublineage in Senegal. In addition, one recombinant BA.4 sequence (505,707_SL) was closer to sequences from Argentina, France and Indonesia, exhibiting that the virus experienced a probable genetic micro-evolution during it spread within this cluster of cases in Northern Senegal I. According to the topology of branches, the newly characterized XAS recombinant sequence (5,055,710_SL) emerged prior to the cluster of BA.4 sequences identified in Saint-Louis and could be the index case of this cluster. In addition, it emerged prior to previously available XAS sequences from Senegal which were collected on July 17, 2022 from outgoing travellers, exhibiting that this sequence represents to date, the first reported XAS sequence of this variant from Senegal (Fig. 1).

Fig. 1.

Fig 1

Open in a new tab

Maximum likelihood (ML) phylogenetic tree of the newly characterized SARS-CoV-2 sequences from the Saint-Louis medical region.

The phylogenetic tree was generated using the maximum likelihood method implemented in the IQ-TREE software for 10,000 Bootstrap replications (Hoang et al., 2018), with the TN+F + I nucleotides substitution as the best-fit model to our dataset (Kalyaanamoorthy et al., 2017). The sequences from Saint-Louis were color-coded in red while the previously available sequences from Senegal were indicated with black dots. The ML tree was unrooted and nodes were supported by Bootstrap values. Bootstrap values below 70% have been hidden.

4. Discussion

Since its first identification in South-Africa in December 2021 (Araf et al., 2022), the Omicron variant has shown high transmissibility and quickly predominated the Delta variant in many countries such as Senegal (Xia et al., 2022).

In Senegal, the increasing prevalence noted from early June 2022 for the BA.4 sublineage (Diagne et al., 2022) among the other identified variants, could be associated with its ability to evade the antibody-mediated protection acquired by vaccination or prior infection (Xia et al., 2022). The monitoring of serological markers and the viral load in YB and her husband revealed a former contact with the SARS-CoV-2 as only IgG were detected and the viral load lasting in 5–7 days.

The predominance of the BA.4 sublineage in members of this cluster of infections confirmed its significant community transmission (Araf et al., 2022), which has led to accumulation of mutations and the emergence of new variants such as the XAS recombinant lineage. The XAS recombinant sequence (505,710_SL) is probably the index case for this SARS-CoV-2 cluster of infections in the Saint-Louis medical region, as this variant has been derived from recombination between the BA.2 and BA.5 sublineages (Focosi et al., 2022) previously described as predominant Omicron variants in Senegal from June to July 2022 (Diagne et al., 2022). In addition, phylogenetic analyses confirmed also that the newly characterized XAS recombinant sequence is the first detected from Senegal to date, considering the date of collection.

Although no clinical impact of these circulating Omicron's recombinant lineages has been reported yet in the country, continuous periodical genomic surveillance in confirmed patients and arriving or outbound travellers, is utmost crucial for not only assessing the emergence of new hybrid variants, but also for understanding virus transmission dynamics, virulence and severity factors to help health authorities take appropriate timely actions for prevention and control of probable future COVID-19 waves or peak of circulations.

Our data revealed not only the circulation of the Omicron BA.4 sublineage in the Saint-Louis medical region, but also the first detection of the XAS recombinant variant in Northern Senegal which represents to date, the first XAS recombinant sequence reported from Senegal. Recombination is one of the essential evolutionary processes that allow new antigenic combinations and altered phenotypes in emerging viruses that might aid the course of cross-species diffusion (Rehman et al., 2020). Our study is noteworthy for the investigation of a cluster of COVID-19 cases in Senegal and by demonstrating the potential for SARS-COV-2 to evolve through recombination, in a micro-scale context such a household. Previous investigations of household clustering have shown its importance for understanding of behaviors associated with secondary transmission during the COVID-19 pandemic (Namageyo-Funa et al., 2022), early identification of close contacts in order to strengthen COVID-19 prevention and control (Yan et al., 2022) and improvement of case management (Ikitimur et al., 2021). Although no evidence of virus importation through international travelling has been reported during investigation of this household cluster, gathering in closed spaces could be the main early driver of transmission (Nsekuye et al., 2021).

In the current context of low virus circulation, the continuous genomic surveillance of SARS-CoV-2 variants is a crucial need and the deployment of more sentinel sequencing labs throughout the country could be promoted for rapid identification of probable future emerging recombinant sub-lineages in Senegal.

Funding source

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors and was only supported by the Institut Pasteur de Dakar.

Ethical approval statement

The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to. The information has not been previously presented in any meeting or conference.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We acknowledge colleagues of virology department at Institut Pasteur de Dakar, Senegal for sharing supportive information necessary for establishment and accomplishment of this study.

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.virusres.2023.199259.

Appendix. Supplementary materials

mmc1.docx (3MB, docx)

Data availability

  • Data will be made available on request.

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Associated Data

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

Supplementary Materials

mmc1.docx (3MB, docx)

Data Availability Statement

  • Data will be made available on request.

Articles from Virus Research are provided here courtesy of Elsevier

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