Invest Clin 65(4): 445 - 453, 2024 https://doi.org/10.54817/IC.v65n4a05

Correspondence author: Laboratorio de Virología Molecular, Centro de Microbiología y Biología Celular, Ins-

tituto Venezolano de Investigaciones Científicas, Caracas, Miranda, Venezuela. E-mail: fhpujol@gmail.com;

Tel.+58.2125041623

Epidemiological and virological

characterization of mpox cases in Venezuela

during the multinational 2022-2023

outbreak.

Pierina D´Angelo

*, Carmen Loureiro

*, Rossana Jaspe

, Yoneira Sulbarán

Lieska Rodríguez

, Víctor Alarcón

, Iraima Monsalve

, José Manuel García

José Luis Zambrano

, Héctor Rangel

, and Flor H Pujol

Dirección General de Diagnóstico, Instituto Nacional de Higiene “Rafael Rangel”,

Caracas, Miranda, Venezuela.

Laboratorio de Virología Molecular, Centro de Microbiología y Biología Celular,

Instituto Venezolano de Investigaciones Científicas, Caracas, Miranda, Venezuela.

Dirección General de Epidemiología, Ministerio del Poder Popular para la Salud,

Caracas, Miranda, Venezuela.

Laboratorio de Virología Celular, Centro de Microbiología y Biología Celular, Instituto

Venezolano de Investigaciones Científicas, Caracas, Miranda, Venezuela.

*Contributed equally.

Keywords: mpox; poxvirus; monkeypox; outbreak; Venezuela.

Abstract. Mpox (formerly known as monkeypox) is an infectious disease

caused by MPXV, a member of the family Poxviridae. On July 23, 2022, the WHO

declared the first Public Health Emergency of International Concern of Mpox due

to an escalating global outbreak with low intensity. Two clades of MPXV and sev-

eral lineages within each of these clades have been described. Clade I, also known

as the Central African clade, causes a more severe and lethal disease than clade

II, which circulates in West Africa. MPXV clade IIb caused the first international

outbreak (2022), while clade Ib caused a more recent one (2023-2024). Venezue-

la reported 12 cases during the 2022-2023 outbreak. This study aims to describe

the epidemiological and virological characteristics of these cases. The first three

cases were from men infected outside Venezuela, while most of the subsequent

ones were from men who acquired the disease in the country. All the cases were

from men who have sex with men, and frequently also people living with HIV-1/

AIDS. No critical outcome was observed in any of the patients. Sequence analysis

showed that most of the MPXV belonged to clade IIb lineage B.1. The recurrent

emergence of mpox epidemics warrants the further implementation of molecular

epidemiology surveillance and vaccination programs.

446 D´Angelo et al.

Investigación Clínica 65(4): 2024

Caracterización epidemiológica y virológica de los casos de

mpox en Venezuela durante el brote multinacional 2022-2023.

Invest Clin 2024; 65 (4): 445 – 453

Palabras clave: mpox; poxvirus; viruela símica; brote; Venezuela.

Resumen. La mpox (antes conocida como viruela símica) es una enferme-

dad infecciosa causada por el virus MPXV, miembro de la familia Poxviridae. El

23 de julio de 2022, la OMS declaró la primera Emergencia de Salud Pública de

Importancia Internacional de mpox, debido a un brote mundial en escalada, ac-

tualmente de baja intensidad. Se han descrito dos clados de MPXV y varios linajes

dentro de cada uno de estos clados. El clado I, también conocido como clado

centroafricano, causa una enfermedad más grave y letal que el clado II, el que

circula en África occidental. El primer brote internacional (2022) fue causado

por el clado IIb de MPXV, mientras que uno más reciente (2023-2024) es causado

por el clado Ib. Venezuela notificó 12 casos durante el brote de 2022-2023. El

objetivo de este estudio es describir las características epidemiológicas y virológi-

cas de estos casos. Los primeros tres casos fueron de hombres que se infectaron

fuera de Venezuela, mientras que la mayoría de los siguientes fueron de hombres

que adquirieron la enfermedad en el país. Todos los casos fueron de hombres que

tuvieron sexo con hombres y que viven con VIH-1/SIDA. No se observó ningún

desenlace crítico en ninguno de los pacientes. El análisis de secuencias mostró

que la mayoría de los MPXV pertenecían al linaje B.1 del clado IIb. La aparición

recurrente de epidemias de mpox justifica una mayor implementación de progra-

mas de vacunación y vigilancia epidemiológica molecular.

Received: 17-10-2024 Accepted: 31-10-2024

INTRODUCTION

Mpox (formerly known as monkeypox)

is an infectious disease caused by MPXV, a

member of the Poxviridae family. MPXV be-

longs to the genus Orthopoxvirus. MPXV is

an enveloped 200-250 nm virus with linear

double-stranded DNA of approximately 200

kb. MPXV interacts with glycosaminoglycans

at the surface of the susceptible cells to en-

ter and replicate in the cytoplasm of the in-

fected cell

1-3

This infection causes a variety of clini-

cal manifestations, particularly skin lesions

and lymphadenopathy, but also can present

with musculoskeletal pain, ocular manifesta-

tions, and malaise

. The infection spreads

mainly through contact with infected hu-

mans or animals or contaminated materi-

als. However, frequent cases and deaths have

been observed in children, suggesting that

routes of transmission other than sexual

contact may also be effective in this new out-

break

5,6

. The likelihood of aerosol transmis-

sion seems to be low

The disease has been known to infect

humans since 1970. Several cases have been

reported in Africa since then, with a few

documented cases until 2022 in other coun-

tries outside the continent, primarily due

to zoonotic transmission. On July 23, 2022,

the WHO declared the first public health

emergency of international concern of mpox

due to an escalating global outbreak, which

Mpox cases in Venezuela 447

Vol. 65(4): 445 - 453, 2024

is still ongoing at present, with low intensi-

2,8

. By August 2024, nearly 100,000 cases

have been reported in 122 countries, with

a relatively low mortality rate (207 deaths)

. This outbreak has been characterized by

human-to-human transmission, frequently

among men who have sex with men (MSM).

HIV co-infection is also frequent

On August 14, 2024, the WHO declared

a second public health emergency of interna-

tional concern for mpox due to an ongoing

global outbreak, this time developing in Af-

rica, with the majority of cases in the Demo-

cratic Republic of Congo

4,10

. By the end of

August 2024, the only cases described out

of Africa were in Sweden and Thailand, with

a history of travel from Africa. Both viral

sequences were already available in the GI-

SAID database on August 28, 2024

Two clades of MPXV and several lineag-

es within each of these clades have been de-

scribed. Clade I, also known as the Central

African clade, is associated with higher se-

verity and lethality (up to 10%) compared to

clade II, which circulates in West Africa

12-14

MPXV clade IIb caused the first internation-

al outbreak (2022), while the more recent

one is caused by clade Ib.

The USA exhibited the highest number

of mpox cases of the first outbreak world-

wide: more than 33,000 by August 2024. In

Latin America, Brazil, Colombia, Mexico,

and Peru, there was also a high number of

cases: more than 11,000 cases in Brazil,

more than 4000 cases in Colombia and Mex-

ico, and more than 3,500 cases in Peru until

August 2024

Venezuela reported 12 cases during the

2022 outbreak

15,16

. This study aims to de-

scribe the epidemiological and virological

characteristics of these cases.

MATERIALS AND METHODS

This is a descriptive study of the cases

of mpox detected in Venezuela. The Instituto

Nacional de Higiene Rafael Rangel (INHRR)

is responsible for the molecular diagnosis of

MPXV in Venezuela. It implemented an algo-

rithm for the molecular detection of MPXV

cases, previously discarding other confusing

exanthema-inducing infections, Varicella-

Zoster and Herpesvirus, by detecting IgM/

IgG antibodies in the sera of suspected pa-

tients

. The presence of MPXV DNA was de-

tected by qPCR, as previously described

Based on the WHO/PAHO recommendations

on strengthening surveillance, the country

has decentralized molecular diagnosis since

January 2023 into four states, and surveil-

lance was intensified through the use of the

Vesicular Eruptive Febrile Syndrome surveil-

lance protocol.

Once qRT-PCR identified the cases,

MPXV genomic DNA was amplified using

ARTIC primers

for complete genome se-

quencing. Multiple libraries were prepared

from the same sample to increase sequence

coverage, using the DNA Prep library prepa-

ration kit with the Nextera DNA CD Indexes

(Illumina, Inc. San Diego, CA, USA) for next-

generation sequencing (NGS). The librar-

ies were pooled and quantified (Qubit DNA

HS, Thermo Scientific, Waltham, MA, USA).

Their quality was checked (Bio-Fragment An-

alyzer, Qsep1-Lite, BiOptic, New Taipei City,

Taiwan) before sequencing, and sequencing

was carried out using an iSeq 100 platform

and a 300-cycle V2 kit with paired-end se-

quencing.

The viral genome sequence assembly

was performed using the Genome Detective

Virus tool (https://www.genomedetective.

com/). Nucleotide sequences of three par-

tial complete genomes with more than 60%

coverage have been deposited into the GI-

SAID database with the accession IDs EPI_

ISL_15014548 and EPI_ISL_19370098. The

other two sequences (MPXV6 and MPXV10),

with lower coverage and are not acceptable

for GISAID, are available upon request.

FASTA file obtained from Genome De-

tective was analyzed using the Nextclade

web tool Nextclade Web 1.14.1 (https://

clades.nextstrain.org). MPXV genomes were

aligned using MAFFT v.7 (https://mafft.cbrc.

448 D´Angelo et al.

Investigación Clínica 65(4): 2024

jp/alignment/server/). Mega

was used for

sequence identity determination.

RESULTS

Twelve cases of mpox were reported in

Venezuela between June 2022 and March

2023 (Table 1). Five corresponded to im-

ported cases, and seven were community-

acquired. All patients were male, acquired

through sexual contact (MSM), and 7/10

(70%) corresponded to people living with

HIV-1/AIDS (PLWHA). The mean age was 30

years (range 24-37). Most of the cases corre-

sponded to the capital region, 42% (5/12) of

the Bolivarian State of Miranda, 25% (3/12)

of the Capital District, and the remaining 8%

one each from Barinas, Carabobo, Guarico

and Zulia states (Table 1).

A complete genome sequence could be

obtained for only one isolate (MPXV7, with

92.7% coverage), while partial sequences

were obtained for three more isolates (Table

2). Even with the low coverage, it could be

confirmed that all isolates were from MPXV

clade IIb. A discrepancy was found for the

isolate MPXV1 for lineage assignment be-

tween the different web algorithms available

online (Table 2).

Most MPXV isolates detected in Vene-

zuela belonged to the B.1 lineage. Ten thou-

sand three hundred fifty-four total sequences

were available in the GISAID database until Au-

gust 29, 2024

. From these, 8868 sequences

belong to the B.1 lineage and its sublineages

(3848 to the B.1 lineage and 5020 to the B.1.1

to the B.1.22 sublineages), being the B.1 lin-

eage prevalent globally during the first interna-

tional outbreak of mpox.

The MPXV1 isolate was classified as lin-

eage B.1 by Nextclade, as were most isolates

from this study, but B.1.6 by GISAID

. The

B.1.6 assignment by GISAID is somehow

unexpected since this lineage is strongly

associated with mpox cases in Peru

, and

the country of infection for patient C1 was

Spain.

Five hundred thirty-three B.1.6 MPXV

sequences were available at GISAID on Au-

gust 29, 2024

(5.1% of the total sequenc-

es). Of the 439 B.1.6 sequences (82%) were

from Peru (Fig. 1). Some B.1.6 isolates were

also found in Colombia and Chile, while this

isolate was utterly absent from Brazil (0/353

sequences), Bolivia (No MPXV sequence

available), Argentina (0/11 sequences) and

only 1/102 B.1.6 isolates in Ecuador. How-

Table 1

Demographic characteristics of patients infected with MPXV reported in Venezuela in 2022.

Patient ID Sex and age Date of diagnosis Travel from MSM HIV-1 Outcome

C1 Male, 32 12/6/22 Spain Yes Negative Good

C2 Male, 28 25/8/22 Brazil Yes Positive Good

C3 Male, 31 23/8/22 Peru Yes Negative Good

C4 Male, 24 10/9/22 None Yes Positive Good

C5 Male, 30 6/9/22 None Yes Positive Good

C6 Male, 36 19/9/22 None Yes Positive Good

C7 Male, 31 20/9/22 None Yes Positive Good

C8* Male, 37 23/9/22 None Yes N/A** Good

C9* Male, 25 26/9/22 None Yes N/A Good

C10 Male, 30 13/10/22 Colombia Yes N/A Good

C11 Male, 26 9/12/22 None Yes Positive Good

C12 Male, 33 3/3/23 Panamá Yes Positive Good

*Reported contact with patient C7. **N/A: not available. Did not reported HIV status nor accepted an HIV test.

Mpox cases in Venezuela 449

Vol. 65(4): 445 - 453, 2024

ever, the earliest sequences for this lineage

(earliest collection date June 5, 2022) were

from the Netherlands, where 24/182 se-

quences (13%) were classified as B.1.6 by

the GISAID database: the earliest collection

date of B.1.6 isolates from Peru was June 25

of this year (from the first reported case in

the country). Then, it cannot be discarded

that the B.1.6 lineage was also circulating

in Spain in June 2022 and not detected

because of the relatively low number of se-

quences available from this country (n=78).

Another Venezuelan isolate was clas-

sified as B.1.19 by Nextclade (from patient

C6). No information on lineage classification

can be obtained from the GISAID database

since this sequence could not be submitted

due to low coverage (Table 2). A total of 58

sequences of the B.1.19 lineage were avail-

able on the GISAID database

, making it a

lineage with a low detection frequency. Most

of the sequences are from Europe (n=39),

18 from North America, and none have been

reported in South America. However, the

Table 2

Sequence analysis of MPXV Venezuelan isolates.

Isolate ID* Patient ID Accession ID Genome coverage** Clade Lineage***

MPXV1 C1 EPI_ISL_15014548 64.2 % IIb B.1 or B.1.6

MPXV6 C6 NA**** 37.3 % IIb B.1.19

MPXV7 C7 EPI_ISL_19370098 92.7 % IIb B.1

MPXV8 C8 NA**** 56.8 % IIb B.1

MPXV10 C10 NA**** 39.0 % IIb B.1

*For the other MPXV isolates, sequence information could not be obtained. **Percent nucleotides effectively

sequenced along the whole genome. ***Lineage assignment according to the Nextclade algorithm. In the case

of MPXV1, GISAID assigned this isolate to the B.1.6 lineage. ****NA: not available. Not submitted to GISAID

because of low coverage.

Fig. 1. Distribution of the MPXV lineage B.1.6 in the world. (GISAID, 2024).

450 D´Angelo et al.

Investigación Clínica 65(4): 2024

classification of this Venezuelan isolate as

B.1.19 may be misleading because of the low

coverage of this sequence.

The partial sequence of MPXV8 dis-

played more than 99.99% identity with the

MPXV7 sequence, which agrees with the his-

tory of contact between patients C7 and C8

(Table 1).

DISCUSSION

Relatively few cases of mpox were re-

ported in Venezuela. Comegna et al., 2023

suggested several factors to explain the low

number of reported cases, including limited

diagnostic capacity, particularly outside the

capital city. However, as stated before, 4/12

cases were from states outside the capital

region, and four diagnostic centers were per-

forming molecular diagnosis of mpox in other

states. The fact that many of the community-

acquired cases in Venezuela were also PLWHA

suggests that the fear of discrimination may

have played a role in the low number of cases

detected in the country. In addition, the lack

of knowledge about this disease (both among

patients and among health workers who are

not trained to detect cases) may have ham-

pered the identification of cases. Finally, as

this outbreak often presented with a mild dis-

ease with low severity and cryptic manifesta-

tions, often in the genital area, many cases

may have gone undetected

. Since PLWHA

are more likely to seek medical care, with

physicians aware of this disease, this increases

the likelihood of detecting mpox cases. Most

of the MPXV reported in Venezuela belonged

to clade IIb lineage B.1.

The high number of mpox cases asso-

ciated with the first international outbreak

led to the evolution of this virus, with the

subsequent emergence of lineages inside the

clade IIb

. An example of this is the emer-

gence of lineage B.1.6, which seems to have

emerged in Peru

. The importance of ge-

nomic surveillance has been stressed with

the COVID-19 pandemic. However, the con-

tribution of MPXV genomic sequences to

the GISAID database was not proportional

to each country’s mpox cases

. The genome

length of this DNA virus (almost 200.000

base pairs) does not contribute to facilitat-

ing this task. Only one complete genome

with satisfactory coverage could be obtained

in our case. The analysis of these complete

or partial genomic sequences allowed us to

determine the circulation of the lineage B.1

of the clade IIb in the country.

As of the end of October 2024, only three

cases of the second mpox outbreak (clade Ib)

have been reported outside Africa (with a

previous history of being in that continent)

9,10,22

. This second outbreak did not threaten

public health in Latin America by the end of

2024. However, the recurrent outbreaks of

this disease have shown the emergence of vi-

ral lineages with increased ability of human-

to-human transmission

. This warrants the

need for enhancing response interventions

and surveillance systems, targeted vaccina-

tion, such as vaccination of high-risk individu-

als, persons in contact with mpox cases, ring

vaccination in endemic areas

5,24,25

, and edu-

cational campaigns on mpox

24,25

ACKNOWLEDGEMENTS

To the Health Personnel who treated

mpox cases effectively and accurately in the

country.

Funding

This project was funded by the Minis-

terio del Poder Popular para Ciencia y Tec-

nología de Venezuela (MINCYT).

Conflict of competence

The authors declare that they have no

conflict of competence.

ORCID numbers of authors

• Pierina D´Angelo (PA):

0000-0002-1658-6128

• Carmen L. Loureiro (CL):

0000-0003-3665-1107

Mpox cases in Venezuela 451

Vol. 65(4): 445 - 453, 2024

• Rossana C Jaspe (RCJ):

0000-0002-4816-1378

• Yoneira Sulbaran (YS):

0000-0002-3170-353X

• Lieska Rodríguez (LR):

0009-0002-6721-855X

• Víctor Alarcón (VA):

0000-0002-4418-6690

• Iraima Monsalve (IM):

0009-0005-2620-7944

• José Manuel García (JMG):

0000-0002-2152-0887

• José Luis Zambrano (JLZ):

0000-0001-9884-2940

• Héctor R Rangel (HRR):

0000-0001-5937-9690

• Flor H. Pujol (FHJ):

0000-0001-6086-6883

Contributions of authors

Substantial contribution to the concep-

tion and design of the study; Critical review

of the article; Approval of the final version

to be published (all authors). PA: Data col-

lection and molecular diagnosis of cases.

CL: Amplification of the viral genome for

sequencing. RCJ y YS: Next-generation se-

quencing. LR,VA,IM, JMG: Data collection

and epidemiological analysis of cases. JLZ:

Critical review of the manuscript and de-

sign of the figure. HRR: Critical review of

the study and manuscript. FHJ: Supervision

of the study; Writing the first version of the

manuscript.

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