Citation: Ismael, N.; Wilkinson, E.;
Mahumane, I.; Gemusse, H.;
Giandhari, J.; Bauhofer, A.; Vubil, A.;
Mambo, P.; Singh, L.;
Mabunda, N.; et al. Molecular
Epidemiology and Trends in HIV-1
Transmitted Drug Resistance in
Mozambique 1999–2018. Viruses 2022,
14, 1992. https://doi.org/10.3390/
v14091992
Academic Editor: Orna Mor
Received: 29 July 2022
Accepted: 5 September 2022
Published: 9 September 2022
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viruses
Article
Molecular Epidemiology and Trends in HIV-1 Transmitted Drug
Resistance in Mozambique 1999–2018
Nalia Ismael
1,2,
*, Eduan Wilkinson
3
, Isabel Mahumane
1
, Hernane Gemusse
1
, Jennifer Giandhari
4
,
Adilson Bauhofer
1
, Adolfo Vubil
1
, Pirolita Mambo
1
, Lavanya Singh
4
,Nédio Mabunda
1
, Dulce Bila
5
,
Susan Engelbrecht
2
, Eduardo Gudo
1
, Richard Lessells
4
and Túlio de Oliveira
3,
*
1
Instituto Nacional de Saúde (INS), Estrada Nacional N1, Marracuene 3943, Mozambique
2
Division of Medical Virology, Faculty of Medicine and Health Sciences, Stellenbosch University,
Cape Town 8000, South Africa
3
Centre for Epidemic Response and Innovation (CERI), School of Data Science and Computational Thinking,
Stellenbosch University, Stellenbosch 7602, South Africa
4
KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and
Medical Sciences, University of KwaZulu-Natal, Durban 4000, South Africa
5
Elizabeth Glaser Pediatric AIDS Foundation in Mozambique, Avenida Agostinho Neto,
Maputo 620, Mozambique
* Correspondence: nalia.ismael@ins.gov.mz (N.I.); tulio@sun.ac.za (T.d.O.)
Abstract: HIV drug resistance (HIVDR) can become a public health concern, especially in low- and
middle-income countries where genotypic testing for people initiating antiretroviral therapy (ART) is
not available. For first-line regimens to remain effective, levels of transmitted drug resistance (TDR)
need to be monitored over time. To determine the temporal trends of TDR in Mozambique, a search
for studies in PubMed and sequences in GenBank was performed. Only studies covering the pol
region that described HIVDR and genetic diversity from treatment naïve patients were included.
A dataset from seven published studies and one novel unpublished study conducted between
1999 and 2018 were included. The Calibrated Population Resistance tool (CPR) and REGA HIV-1
Subtyping Tool version 3 for sequences pooled by sampling year were used to determine resistance
mutations and subtypes, respectively. The prevalence of HIVDR amongst treatment-naïve individuals
increased over time, reaching 14.4% in 2018. The increase was most prominent for non-nucleoside
reverse transcriptase inhibitors (NNRTIs), reaching 12.7% in 2018. Subtype C was predominant in all
regions, but a higher genetic variability (19% non-subtype C) was observed in the north region of
Mozambique. These findings confirm a higher diversity of HIV in the north of the country and an
increased prevalence of NNRTI resistance among treatment naïve individuals over time.
Keywords: transmitted; drug; resistance; HIV; molecular epidemiology; Mozambique; mutations;
genetic diversity; treatment naïve; temporal trend
1. Introduction
In response to the HIV epidemic, antiretroviral treatment (ART) roll out has risen
dramatically, with 28.2 million individuals on treatment by 2021 worldwide [1]. Although
ART has substantially reduced HIV related morbidity, mortality, and transmission, HIV
Drug Resistance (HIVDR) can become a problem, particularly in low- and middle-income
countries (LMICs) where genotyping testing is not readily available [2,3]. Among ART
naïve individuals, drug resistance may occur through Transmitted Drug Resistance (TDR)
or Pretreatment HIV Drug Resistance (PDR) which may compromise the success of future
first line regimens [4]. TDR occurs when an uninfected person naïve to antiretrovirals
(ARVs) is infected with a resistant virus and PDR defined as resistance being detected
among people initiating treatment or reinitiating first-line regimen after being exposed to
ARVs [5].
Viruses 2022, 14, 1992. https://doi.org/10.3390/v14091992 https://www.mdpi.com/journal/viruses