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1
salud pública de méxico
SARS-CoV-2 variants in US-Mexico border
Artículo originAl
Chaillon A, Bojorquez I, Sepulveda J,
Harvey-Vera AY, Rangel MG, Skaathun B, Mehta SR,
Ignacio C, Porrachia M, Smith DM, Strathdee SA.
Cocirculation and replacement of SARS-CoV-2
variants in crowded settings and marginalized
populations along the US-Mexico border.
Salud Publica Mex. 2022.
https://doi.org/10.21149/13980
Chaillon A, Bojorquez I, Sepulveda J,
Harvey-Vera AY, Rangel MG, Skaathun B, Mehta SR,
Ignacio C, Porrachia M, Smith DM, Strathdee SA.
Cocirculación y reemplazo de variantes de SARS-CoV-2
en espacios hacinados y poblaciones marginadas
en la frontera México-EUA.
Salud Publica Mex. 2022.
https://doi.org/10.21149/13980
Cocirculation and replacement of
SARS-CoV-2 variants in crowded settings
and marginalized populations along
the US-Mexico border
Antoine Chaillon, MD, PhD,(1) Ietza Bojorquez, MSc, PhD,(2) Jaime Sepulveda, MPH, DSc,(3)
Alicia Yolanda Harvey-Vera, MD, PhD,(1,4,5) M Gudelia Rangel, MPH, PhD,(2,5) Britt Skaathun, MPH, PhD,(1)
Sanjay R Mehta, MD,(1,6) Caroline Ignacio, BSc,(1) Magali Porrachia, MS,(1) Davey M Smith,MD, MAS,(1,6)
Steffanie A Strathdee, PhD.(1)
(1) Division of Infectious Diseases and Global Public Health, University of California San Diego. San Diego, United States.
(2) Departamento de Estudios de Población, El Colegio de la Frontera Norte. Tijuana, Mexico.
(3) Institute for Global Health Sciences, University of California. San Francisco, United States.
(4) Facultad de Medicina, Universidad de Xochicalco. Tijuana, Mexico.
(5) United States-Mexico Border Health Commission. Tijuana, Mexico.
(6) Veterans Affairs Health System. San Diego, United States.
Received on: June 20, 2022 • Accepted on: October 13, 2022 • Published online: December 7, 2022
Corresponding author: Ietza Bojorquez. El Colegio de la Frontera Norte. Carretera Escénica Tijuana-Ensenada,
San Antonio del Mar. 22560 Tijuana, Baja California, Mexico.
email: ietzabch@colef.mx
License: CC BY-NC-SA 4.0
Abstract
Objective. To interrogate the circulating SARS-CoV-2 lin-
eages and recombinant variants in persons living in migrant
shelters and persons who inject drugs (PWID). Materials
and methods. We combined data from two studies with
marginalized populations (migrants in shelters and persons
who inject drugs) in Tijuana, Mexico. SARS-CoV-2 variants
were identied on nasal swabs specimens and compared to
publicly available genomes sampled in Mexico and California.
Results. All but 2 of the 10 lineages identied were predomi-
nantly detected in North and Central America. Discrepan-
cies between migrants and PWID can be explained by the
temporal emergence and short time span of most of these
lineages in the region. Conclusion. The results illustrate the
temporo-spatial structure for SARS-CoV-2 lineage dispersal
and the potential co-circulation of multiple lineages in high-
Resumen
Objetivo. Investigar los linajes circulantes y variantes
recombinantes de SARS-CoV-2 en migrantes en albergues y
usuarios de drogas inyectables (UDI). Material y méto-
dos. Se combinaron datos de dos estudios con poblaciones
marginadas (migrantes en albergues y UDI) en Tijuana, México.
Se identicaron variantes de SARS-CoV-2 en exudado nasal
y se compararon con genomas disponibles públicamente de
muestras de México y California. Resultados. Ocho de 10
linajes identicados se detectaron principalmente en Norte y
Centro América. Las discrepancias entre migrantes y UDI se
pueden explicar por la emergencia temporal y la corta dura-
ción de la mayoría de estos linajes en la región. Conclusión.
Los resultados ilustran la estructura temporo-espacial de la
dispersión de linajes de SARS-CoV-2, y la circulación posible
de linajes múltiples en poblaciones en riesgo con contactos
Artículo originAl
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Chaillon A y col.
Mobility data can be used to predict the spread of
SARS-CoV-21-3 and other viruses.4 The successive
emergence of SARS-CoV-2 variants of concern (VOC)
and their rapid spread around the world has highlighted
the importance of genomic surveillance. For example,
the B.1.1.529 variant aka ‘Omicron’ was rst reported
to the World Health Organization (WHO) from South
Africa on 24 November 2021 and has been character-
ized by key mutations in the S protein, which play an
integral role in viral transmission, immune evasion and
virulence. Another mechanism for viral evolution is
recombination. For recombination to occur, the paren-
tal lineages need to cocirculate in the same location to
allow specic individuals to become coinfected. This
scenario provides the circumstances during which chi-
meric genotypes can emerge. For SARS-CoV-2, the rst
recombinant lineage in the Pango nomenclature system5
was designated as lineage XA after being identied in
the UK. Since then, many other recombinants have been
identied and led to limited or more global outbreaks.
For example, XB variant6 (aka B.1.628), a recombinant
lineage with parental lineage B.1.634 and B.1.631, was
rst identied in Mexico which also spread to the US,
Guatemala, Honduras and El Salvador. The widespread
circulation of lineage XB and other recombinants across
multiple countries over an extended time span raised
important questions regarding the role and potential
eects of recombination on the evolution of SARS-CoV-2
during the ongoing Covid-19 pandemic.
The Covid-19 pandemic has disproportionately
impacted socially marginalized populations.7 In this
context, migrant populations living in temporary accom-
modations like camps and shelters may be at high risk
for virus co-circulation and potential emergence of new
VOC. Of particular concern are in-transit migrants, refu-
gees, and asylum seekers, and those residing in camps
and other overcrowded settings with limited access to
resources for hygiene or physical distancing. Migrants
in such settings typically have limited access to health-
care, employment, and social services, and are therefore
vulnerable to the social and economic impacts of lock-
down and other measures.8-10 We recently reported that
the prevalence of SAR-CoV-2 RNA positive samples
among migrants to Tijuana living in shelters during
2021 was low (1.5%) but half (53.0%) were SARS-CoV-2
seropositive.11 The high rate of social interactions within
temporary accommodation and outside (e.g. in public
transportation) and the mobility of these populations
are important risk factors for cocirculation of dierent
lineages and potential recombination.
Similarly, the Covid-19 pandemic has disproportion-
ally impacted other vulnerable and marginalized com-
munities, such as people who use drugs (PWUD).12-14 In
a study of people who inject drugs (PWID) in Tijuana
and San Diego, California conducted from 2020-2021,
SARS-CoV-2 seroprevalence was 37.%.15 Cross-border
mobility and forced deportation has also been found
to heighten vulnerability to a range of health and social
harms in the Mexico-US border region, such as HIV and
tuberculosis.16-20
Herein, we report upon SARS-CoV2 variants circu-
lating in high risk and vulnerable populations of PWID
and migrant populations living in temporary accom-
modations in the Mexico-US border region during the
Covid-19 pandemic, and interrogate the cocirculation
of these variants in Mexico and neighboring California.
Materials and methods
Cohort description and sampling
EPICO study. A non-probability survey of adult mi-
grants aged ≥18 years living in shelters was conducted
from November–December 2020 and February-April
2021. Participants (N=598) underwent interviewer-
administered surveys in Spanish, English or French,
and provided anterior nasal swabs for SARS-CoV-2
RNA testing.
La Frontera study. Between October 2020 and September
2021 PWID within the last month who were aged ≥18
years were recruited through community outreach in
Tijuana (N=200) and San Diego (N=400). The Tijuana
sample and half of the San Diego sample were required
to reside in either city but report not having ever crossed
the US-Mexico border to inject drugs, whereas the re-
maining half of the San Diego sample was required to
have injected drugs in Mexico within the last two years.
Participants underwent interviewer-administered sur-
veys in Spanish or English and provided anterior nasal
risk populations with close social contacts. These conditions
create the potential for recombination to take place in the
California-Baja California border.
Keywords: SARS-CoV-2; lineages; recombination, genetic; drug
users; emigrants and immigrants
sociales estrechos. Estas condiciones generan el potencial
de recombinación en la frontera California-Baja California.
Palabras clave: SARS-CoV-2; linajes; recombinación genética;
usuarios de drogas; migrantes
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SARS-CoV-2 variants in US-Mexico border
Artículo originAl
swabs for SARS-CoV-2 RNA testing at enrolment and
six months later.
Pre- and post-test counseling was provided follow-
ing national guidelines in the U.S. and Mexico. For both
studies, samples were batched and stored at -80 degrees
Celsius and shipped weekly on dry ice for SARS-CoV-2
RNA detection.
SARS-CoV-2 detection and sequencing. Qualitative tests
for SARS-CoV-2 were performed on all collected nasal
swabs specimen for SARS-CoV-2 RNA detection using the
FluxErgy platform (Irvine, CA, USA). SARS-CoV-2 full
genome sequencing was performed using the Covid-19
ARTIC v4 Illumina library construction and sequenc-
ing protocol (https://github.com/CDCgov/SARS-
CoV-2_Sequencing). Amplicons were generated with
the NEBNext VarSkip VSS2b Primer kit ( https://github.
com/nebiolabs/VarSkip). PCR conditions were 98°C for
30 s, followed by 35 cycles of 95°C for 15s and 63°C for 5
min. Libraries were generated with the NEBNext ARTIC
SARS-CoV-2 FS Library prep kit (Illumina) with NEBNext
Multiplex Oligos for Illumina. Samples were sequenced
using a 2 x 75bp paired-end reads. Reads were processed
with the CLC Genomics Workbench V22 (Qiagen). Briey
the workow identies individual SARS-CoV-2 sample
variants by rst trimming and mapping high quality
reads (>20) to the reference genome and then calling vari-
ants to generate a full genome consensus for each sample.
Lineage identication and analyses. We used the Phyloge-
netic Assignment of Named Global Outbreak Lineages
(Pangolin) (version 1.1.14) command-line tool and Pango
nomenclature system21 to determine the lineage of all
SARS-CoV-2 genomes. Publicly available genomes sam-
pled in Mexico and California from the lineages identied
in the LF and EPICO cohorts were also retrieved from
the Global Initiative on Sharing Avian Inuenza Data
(GISAID) database.22 We employed the Wuhan lineage
as the reference to characterize the isolates.
Ethical considerations. These studies were reviewed and
approved by the ethics committees of the University
of California in San Diego (no. 201153), El Colegio de la
Frontera Norte (no. 066-160720) and Xochicalco Univer-
sity. All participants gave written informed consent in
their preferred language (Spanish, French or English).
Results
Cohort and sampling
EPICO study. Samples were collected from November
to December 2020, and from February to April 2021. Of
598 samples, seven (1.2%) were conrmed positive by
RT-PCR and six were successfully sequenced (gure 1A).
La Frontera study. A total of 1 159 samples (1.4 [min-
max: 1 -3] samples per participant on average) were
collected between December 2020 to January 2022. Nine
of the 1 159 (0.8%) tested positive and were sequenced
(gure 1B).
SARS-CoV-2 genomic analysis
EPICO cohort. During the spring of 2021, three distinct
lineages were detected (from March 27th to April 12th)
(gure 2). All three were most detected in the US and
Mexico. XB recombinant lineage (n=4)23 was rst iden-
tied in July 2020 and March 2021 in California and
Mexico respectively and last reported in September
and August 2021. The two other B1.627 and B1.631 lin-
eages were also most common in in the US and Mexico
followed by Central American countries and were not
detected after August 2021 (tables I and II).5,22,24,25
La Frontera cohort. Seven distinct lineages were identied
from August 19th, 2021 (rst detection), to January 2022
(gure 2). All but AY.42 (considered a large European
[especially Spain] Delta sub-lineage) and BA.1.17.2
(sublineage of worldwide spread BA.1.17 lineage with
S:701V) were also most frequently reported in North
and Central America and co-circulated in California
and Mexico in the summer/fall of 2021.
To interrogate the co-circulation of these lineages
in the Mexico and neighboring California region we
retrieved all full-length genomes available on GISAID.22
The spatial temporal distribution of these lineages
in California and Mexico along with those from the
EPICO and La Frontera cohort are presented in gure
321,26 and under microreact project. A detailed summary
of the distribution of these 10 SARS-CoV-2 lineages is
provided in tables I and II5,22,24,25 and gure 3,21,26 along
with timespan and cumulative prevalence in the United
States, in Mexico and in California, and worldwide. Data
can be visualized under microreact project (https://
microreact.org/project/auby4ddjtcyrfy3q3dxdds).
Discussion
All but 2 of the 10 lineages reported in this study among
PWID and migrants in shelters at the California-Mexico
border were predominantly detected in North and
Central America. The discrepancies between the two
cohorts can be explained by the temporal emergence
and short time span of most of these lineages in the
region. Hence, the three lineages identied among
migrants in shelters (EPICO study) were collected in
Artículo originAl
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Chaillon A y col.
* Positive samples that were further sequenced are shown in red.
Figure 1. Overview OF weekly sampling FOr the epiCO (a) and la FrOntera (B) COhOrt*
Table I
data FrOm weBpage COv-lineage.Org24 retrieved On may 22 2022,
using the pangOlin nOmenClature5
Lineage N. sequences Most common countries
(%) Earliest date # designated # assigned Description
EPICO
B.1.627
1
United States of America (72.0),
Mexico (11.0), El Salvador (7.0),
Honduras (5.0), Guatemala (4.0)
1/9/21 117 474 USA, Mexico and Honduras lineage,
from pango-designation issue #130
B.1.634
1
United States of America (64.0),
Mexico (34.0), Honduras (1.0),
Guatemala (0.0), Panama (0.0)
3/2/21 71 289 Mexico and USA lineage, from
pango-designation issue #159
XB
4
United States of America (77.0),
Mexico (16.0), Guatemala (3.0),
Honduras (2.0), El Salvador (1.0)
7/8/20 729 3 186
Recombinant lineage with parental
lineages B.1.634 and B.1.631,
Central and North America lineage,
discussed in pango-designation issue
#189. Formally B.1.628
(continues…)
150
100
50
0
150
100
50
0
Number of tests per weekNumber of tests per week
A. EPICO
B. La Frontera
Dec 2020 Jan 2021 Feb 2021 Mar 2021 Apr 2021 May 2021 Jun 2021 Jul 2021 Aug 2021 Sep 2021 Oct 2021 Nov 2021 Dec 2021 Jan 2022 Feb 2022 Mar 2022 Apr 2022
Dec 2020 Jan 2021 Feb 2021 Mar 2021 Apr 2021 May 2021 Jun 2021 Jul 2021 Aug 2021 Sep 2021 Oct 2021 Nov 2021 Dec 2021 Jan 2022 Feb 2022 Mar 2022 Apr 2022
Time
Time
Results: Positive Negative
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(continuation)
La Frontera
AY.100
2
United States of America (87.0),
Mexico (4.0), India (1.0), Brazil (1.0),
Canada (1.0)
7/16/20 16 627 86 622 Alias of B.1.617.2.100, USA lineage
AY.119
1
United States of America (95.0),
Germany (1.0), Canada (1.0), United
Kingdom (0.0), Dominican Republic
(0.0)
10/29/20 2 356 35 639 Alias of B.1.617.2.119, USA lineage
AY.20
1
United States of America (58.0),
Mexico (32.0), India (2.0), Germany
(1.0), Colombia (1.0)
1/8/21 2 442 35 116 Alias of B.1.617.2.20, USA and
Mexico lineage
AY.25.1
1
United States of America (55.0), Ca-
nada (40.0), Chile (2.0), Colombia
(1.0), Aruba (0.0)
5/12/20 41 309 12 4153
Alias of B.1.617.2.25.1, Canada and
USA lineage, from pango-designa-
tion issue #313
AY.42
2
Germany (19.0), Spain (17.0),
France (15.0), Switzerland (7.0),
Denmark (6.0)
10/15/20 14 252 26 326
Alias of B.1.617.2.42, European
lineage, from pango-designation
issue #239
AY.26
1
United States of America (83.0),
Mexico (12.0), Brazil (1.0), Israel
(0.0), Portugal (0.0)
1/7/21 5 011 43 878
Alias of B.1.617.2.26, USA and
Mexico lineage, from pango-desig-
nation issue #188
BA.1.17.2
1
United Kingdom (71.0), United Sta-
tes of America (5.0), Canada (4.0),
Germany (3.0), Denmark (3.0)
10/7/21 30 818 18 6393 Alias of B.1.1.529.1.17.2, lineage
from pango-designation issue #462
Table II
lineage assignment OF the 15 genOmes FrOm the epiCO (n=6) and la FrOntera (n=9)
and timespan OF sampling distriButiOn in the united states, CaliFOrnia,
usa and mexiCO. data FrOm the gisaid22
Lineage n Location Total Cum. prevalence*
%
First‡Last§
EPICO
B1.627 1 Mexico 51 < 0.5 4-Mar-21 21-Jul-21
California, US 72 < 0.5 3-Feb-21 21-Jul-21
United States 361 < 0.5 16-Jan-21 15-Aug-21
Worldwide 493 < 0.5 9-Jan-21 21-Aug-21
B1.634 1 Mexico 96 < 0.5 9-Apr-21 30-Jul-21
California, US 21 < 0.5 12-Apr-21 11-Aug-21
United States 184 < 0.5 2-Mar-21 16-Aug-21
Worldwide 284 < 0.5 27-Dec-20 16-Aug-21
X.B 4 Mexico 513 1 19-Mar-21 24-Aug-21
California, US 876 < 0.5 8-Jul-20 15-Sep-21
United States 2 627 < 0.5 8-Jul-20 9-Jan-22
Worldwide 3 369 < 0.5 8-Jul-20 15-Feb-22
La Frontera
AY100 2 Mexico 3 107 5 22-Sep-20 16-Feb-22
California, US 12 480 2 31-Aug-20 29-Mar-22
United States 80 611 3 31-Aug-20 29-Mar-22
Worldwide 92 241 1 31-Aug-20 29-Mar-22
(continues…)
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Chaillon A y col.
spring 2021. The lineages B1.627 and B1.634 emerged
in March-April 2021 in both California and Mexico
and were no longer detected worldwide after August
2021. Recombinant lineage X.B (originating from a
recombination event between a B.1.631 major virus
and a lineage B.1.634) was rst reported in California
during the summer 2020 but only in March 2021 in
Mexico. While the widespread circulation of lineage XB
across multiple countries lasted over a longer timespan
worldwide, it was not reported after August/Septem-
ber 2021 in the region.
Seven distinct lineages were identified among
PWID enrolled in the La Frontera cohort. These lin-
eages were detected over a longer timespan than the
previously mentioned lineages but all co-circulated in
California and Mexico during 2021.
An important limitation of this observational study
is that we had only a small number of isolates available
for sequencing. Further larger scale studies would be
(continuation)
AY119 1 Mexico 19 < 0.5 2-Aug-21 17-Dec-21
California, US 5 849 1 12-Jun-21 7-Feb-22
United States 34 806 1 14-Jan-21 18-Apr-22
Worldwide 36 777 < 0.5 29-Oct-20 18-Apr-22
AY.20 1 Mexico 11 271 20 21-Jan-21 20-Mar-22
California, US 9 058 2 12-Apr-21 2-Feb-22
United States 20 870 1 14-Jan-21 31-Mar-22
Worldwide 35 985 < 0.5 14-Jan-21 31-Mar-22
AY.25.1 1 California, US 12 352 3 20-Apr-21 7-Feb-22
Mexico 163 < 0.5 29-Jun-21 28-Feb-22
United States 75 346 2 26-Dec-20 24-Mar-22
Worldwide 134 23 1 11-Sep-20 28-Apr-22
AY.42 2 Mexico 14 < 0.5 11-Jul-21 20-Dec-21
California, US 111 < 0.5 1-Jun-21 22-Dec-21
United States 525 < 0.5 1-Jun-21 12-Jan-22
Worldwide 28 786 < 0.5 15-Oct-20 11-Mar-22
AY26 1 Mexico 14 < 0.5 11-Jul-21 20-Dec-21
California, US 111 < 0.5 1-Jun-21 22-Dec-21
United States 525 < 0.5 1-Jun-21 12-Jan-22
Worldwide 28 786 < 0.5 15-Oct-20 11-Mar-22
BA.1.17.2 1 Mexico 102 1 16-Dec-21 31-Mar-22
California, US 1 230 1 1-Dec-21 29-Mar-22
United States 11 155 < 0.5 31-Dec-20 27-Apr-22
Worldwide 196 031 2 23-Oct-20 6-May-22
* Apparent cumulative prevalence is the ratio of the sequences containing B.1.627 to all sequences collected since the identication of B.1.627 in that location.
‡ Dates are based on the sample collection date; §genome key mutations from the outbreak.info25
GISAID: Global Initiative on Sharing Avian Inuenza Data
required to better determine the prevalence trajectories
of these co-circulating variants. However, these results
illustrate the temporo-spatial structure for SARS-CoV-2
lineage dispersal and the potential co-circulation of
multiple lineages in high-risk populations with close
social contacts, conditions for a recombination event to
take place.
Considering the successful worldwide dispersal
of recombinant XB, our study underscores the need
for strengthening the screening, diagnosis, and pre-
vention measures to these vulnerable populations.
It also highlights the potential benet of genomic
sequencing data for quick and informed public health
decisions (e.g. appropriate vaccine response) and the
importance of communication and partnerships at
the regional level. Further studies are necessary to
explore the role and potential eects of recombination
on the evolution of SARS-CoV-2 during the Covid-19
pandemic.
7
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SARS-CoV-2 variants in US-Mexico border
Artículo originAl
Figure 2. mOnthly distriButiOn OF the 10 distinCt lineages identiFied in CaliFOrnia, mexiCO and in
the epiCO and la FrOntera COhOrt
4
3
2
1
0
4
3
2
1
0
4 000
3 000
2 000
1 000
0
6 000
4 000
2 000
0
EPICO
La Frontera
Mexico
California
Apr 2021 Jul 2021 Oct 2021 Jan 2022 Apr 2022
SARS-CoV-2 lineages: AY.100 AY.119 AY.20 AY.25.1 AY.26
AY.42 B.1.627 B.1.634 BA.1.17.2 XB
Sampling date (by month)
Number of genomes
Acknowledgments
We would like to thank the migrant shelters in Tijuana
for facilitating this research, and the participants for
generously contributing their time and experiences.
Data acknowledgements
We gratefully acknowledge the authors, originating
and submitting laboratories of the genetic sequence
and metadata made available through GISAID on
which this research is based. A full acknowledgement
table can be found with the following EPI_SET-IDs
EPI_SET_20220606sv (https://doi.org/10.55876/
gis8.220606sv); EPI_SET_20220606fw (https://doi.
org/10.55876/gis8.220606fw) and EPI_SET_20220606wx
(https://doi.org/10.55876/gis8.220606wx) in Data
Acknowledgement Locator under GISAID resources
(https://www.gisaid.org/).
Funding
This research was funded by the American Academy of
Arts and Sciences, Rethinking the Humanitarian Health
Response to Violent Conict project, the University of
California, San Francisco and the San Diego Center for
AIDS Research (CFAR), which is funded by the National
Institutes of Health (P30 AI036214). AC is supported by
the James B. Pendleton Charitable Trust and by the San
Diego Center for AIDS Research (SD CFAR), an NIH-
funded program (P30 AI036214), which is supported
by the following NIH Institutes and Centers: NIAID,
NCI, NHLBI, NIA, NICHD, NIDA, NIDCR, NIDDK,
NIGMS, NIMH, NIMHD, FIC, and OAR, the UCOP
(R00RG2725) and by the NIH NIDA (R01DA055491).
The study sponsors had no role in the study design; in
the collection, analysis and interpretation of the data;
in the writing of the report; or in the decision to submit
the paper for publication.
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Declaration of conict of interests. The authors declare that they have no
conict of interests.
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Marker
Size
1
109
280
549
6 024
500 km
1
0
California EPICO La Frontera Mexico
AY.100 AY.119 AY.20 AY.25.1 AY.26
AY.42 B.1.627 B.1.634 BA.1.17.2 XB
A. B.
C.
3 500
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A. Microreact26 display of the geolocation of all genomes with associated lineage inferred by the Pangolin assignment tool.21 B. Distribution of the lineages in
California, in Mexico and in the EPICO and La Frontera cohorts. C. Timeline of the 10 lineages. See also microreact project https://microreact.org/project/
auby4ddjtcyrfy3q3dxdds
Figure 3. spatial tempOral distriButiOn OF the 10 lF/epiCO and la FrOntera lineages in Cali-
FOrnia and mexiCO
9
salud pública de méxico
SARS-CoV-2 variants in US-Mexico border
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