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07 Aug 2024
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Spatial and temporal epidemiology of SARS-CoV-2 virus lineages in Teesside, UK, in 2020: effects of socio-economic deprivation, weather, and lockdown on lineage dynamics

Small-scale study reveals the role of socio-economic deprivation, weather and local versus national health decisions on SARS-3 CoV-2 virus lineage dynamics

Recommended by ORCID_LOGO based on reviews by Samuel Alizon and 2 anonymous reviewers

Each and every one of us will recall the severe acute respiratory syndrome (SARS) coronavirus (CoV-2) pandemic, and the national and international political hesitations in its management. Fall 2019, in the city of Wuhan, Hubei province, China, an outbreak of unusual viral pneumonia due to a new emerging coronavirus named as SARS-CoV-2 started, generating late February a modern pandemic called COVID-19, posing very serious threat to global public health and the world economy (Hu et al. 2021). As we are getting out from this pandemic, and even if viral variants are still circulating, what have we learned and retained from this difficult period, shaking our certainties and reminding us of past images of devastating plagues? The COVID-19 pandemic highlighted the importance of early action, widespread testing, open data sharing, and strong public responses (The Lancet Infectious Diseases 2024). It has also highlighted that the animal origin of SARS-CoV-2 was still unknown and the existence of a reservoir host not really demonstrated (Cohen 2021). Beyond this, the COVID-19 pandemic has also revealed the importance of early and continuous surveillance, also raised questions about the role of meteorological conditions on the dispersion and viability of this virus, and highlighted the devastating effects of social inequality. We all remember some medical doctors who became modern preachers announcing the end of the pandemic because of unfavorable weather conditions coming for viral spread!

However, epidemiological studies analyzing the role of different parameters, and effects of national and regional restrictions at local or regional scales on COVID-19 are still rare. In this investigation entitled “Spatial and temporal epidemiology of SARS-3 CoV-2 virus lineages in Teesside, UK, in 2020: effects of socio-economic deprivation, weather, and lockdown on lineage dynamics”, Moss and collaborators’ aim is to analyze how a range of parameters, using both generalized linear mixed- and Bayesian spatial modeling, affected positive cases in the Teesside subregion of North East England during 2020 (Moss et al. 2024). Also, the authors wanted to understand the impacts of national and local government interventions introduced this year affected disease conditions in this subregion showing high levels of deprivation due to deindustrialisation in the latter half of the 20th century. 

According to Moss et al. (2024), the UK government decided for a heterogenous ”tier” system of local restrictions in England during the second wave associated with a more stringent national lockdown. The intention was to be more responsive and appropriate to the different English local contexts. The authors take us through a detailed statistical analysis to show that disease patterns in Teesside were associated with demographic parameters, social deprivation, weather conditions (essentially temperature) and governmental health interventions. Interestingly, findings lead to the conclusion that local tier interventions by public authorities was less effective at reducing COVID-19 cases in Teesside than a strict, long-term national lockdown.  A closer look at the spatio-temporal dynamics of the eight most common SARS-CoV-2 lineages circulating in Teesside in 2020 reveals complex dynamic behaviours differing to those of the total positive cases, certainly due to environmental and demographic stochasticity, and sublocal heterogenous social and economic conditions.

Overall, we recommend reading this study, which reveals the complexity of dealing with epidemics and pandemics, and highlights the importance of sound national political decisions and difficulties to proceed to local adjustments, i.e. tier system, in epidemic and pandemic control. 

The present recommendation is resulting from thorough reviews produced by Samuel Alizon and two anonymous reviewers, and which I thank very much for their review works here. 

 

References

Jon COHEN. 2021. Prophet in purgatory. Science 374, 1040-1045. https://www.science.org/doi/epdf/10.1126/science.acx9661

Ben HU, Hua GUO, Peng ZHOU, Zheng-Li SHI. 2021. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol 19, 141-54. https://doi.org/10.1038/s41579-020-00459-7 

The Lancet Infectious Diseases. 2024. Have we learned anything? Editorial. The Lancet Infectious Diseases 24, 793. https://doi.org/10.1016/S1473-3099(24)00439-0

E.D. Moss, S.P. Rushton, P. Baker, M. Bashton, M.R. Crown, R.N. dos Santos, A. Nelson, S.J. O’Brien, Z. Richards, R.A. Sanderson, W.C. Yew, G.R. Young, C.M. McCann, D.L. Smith (2024) Spatial and temporal epidemiology of SARS-CoV-2 virus lineages in Teesside, UK, in 2020: effects of socio-economic deprivation, weather, and lockdown on lineage dynamics. medRxiv, ver.5 peer-reviewed and recommended by PCI Infections. https://doi.org/10.1101/2022.02.05.22269279

Spatial and temporal epidemiology of SARS-CoV-2 virus lineages in Teesside, UK, in 2020: effects of socio-economic deprivation, weather, and lockdown on lineage dynamicsE.D. Moss, S.P. Rushton, P. Baker, M. Bashton, M.R. Crown, R.N. dos Santos, A. Nelson, S.J. O’Brien, Z. Richards, R.A. Sanderson, W.C. Yew, G.R. Young, C.M. McCann, D.L. Smith<h4>Background</h4> <p>SARS-CoV-2 emerged in the UK in January 2020. The UK government introduced control measures including national 'lockdowns' and local 'tiers' in England to control virus transmission. As the outbreak continued, new variants ...Epidemiology, Microbiology of infections, One Health, VirusesJean-Francois Guégan Samuel Alizon, Anonymous, Olivier Supplisson2023-08-08 15:28:11 View
29 Jan 2024
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Spring reproductive success influences autumnal malarial load in a passerine bird

Avian Plasmodium parasitaemia as an indicator of reproduction investment

Recommended by ORCID_LOGO based on reviews by Luz García-Longoria and 2 anonymous reviewers

Effects of the seasonal variations on within-host parasitaemia are still not well understood and potentially due to numerous factors, e.g. host and parasite species, host sex or age, or geographical regions. In this study, over three years in Switzerland, Pigeault et al. (2024) collected data on great tits reproductive outputs – laying date, clutch size, fledging success – to determine whether they were associated with avian Plasmodium parasitaemia before (winter), during (spring) and after (autumn) the breeding season. They focused on two lineages from two species: a highly generalist lineage Plasmodium relictum (lineage SGS1; Bensch et al. 2009) and a more specialized lineage Plasmodium homonucleophilum (lineage SW2). As previously found, they showed that parasitaemia level is low during the winter and then increase in spring (Applegate, 1970; Applegate 1971). Spring recurrences have been intensively studied but are still not well understood since many non-exclusive factors can provoke them, i.e environmental stressors, reproductive hormones, co-infections or bites of mosquitoes (Cornet et al. 2014).

Interestingly, the parasitaemia level during the winter before and during the breeding season were not associated to the reproductive success, meaning that birds in their populations with low parasitaemia during the winter had not more fledglings than the ones with a higher parasitaemia. However, the individuals who invested the most in the reproduction with a higher number of fledglings had also a higher parasitaemia in the following autumn. The number of laid eggs was not associated with the parasitaemia during the following autumn, showing that the initial investment in the reproduction is less important than the parental care (e.g. chicks feeding) in terms of mid/long term cost. The originality here is that authors followed populations during three periods of the year, which is not an easy task and rarely done in natural populations. Their results highlight the mid/long-term effect of higher resource allocation into reproduction on individuals’ immune system and ability to control parasite replication. Further analyses on various lineages and bird populations from other geographical regions (i.e. different latitudes) would be the next relevant step.

References

Applegate JE (1971) Spring relapse of Plasmodium relictum infections in an experimental field population of English sparrows (Passer domesticus). Journal of Wildlife Diseases, 7, 37–42. https://doi.org/10.7589/0090-3558-7.1.37

Applegate JE, Beaudoin RL (1970) Mechanism of spring relapse in avian malaria: Effect of gonadotropin and corticosterone. Journal of Wildlife Diseases, 6, 443–447. https://doi.org/10.7589/0090-3558-6.4.443

Bensch S, Hellgren O, Pérez‐Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources, 9, 1353-1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

Cornet S, Nicot A, Rivero A, Gandon S (2014) Evolution of plastic transmission strategies in avian malaria. PLoS Pathogens, 10, e1004308. https://doi.org/10.1371/journal.ppat.1004308

Pigeault R, Cozzarolo CS, Wassef J, Gremion J, Bastardot M, Glaizot O, Christe P (2024) Spring reproductive success influences autumnal malarial load in a passerine bird. bioRxiv ver 3. Peer reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.07.28.550923

Spring reproductive success influences autumnal malarial load in a passerine birdRomain Pigeault, Camille-Sophie Cozzarolo, Jérôme Wassef, Jérémy Gremion, Marc Bastardot, Olivier Glaizot, Philippe Christe<p>Although avian haemosporidian parasites are widely used as model organisms to study fundamental questions in evolutionary and behavorial ecology of host-parasite interactions, some of their basic characteristics, such as seasonal variations in ...Interactions between hosts and infectious agents/vectors, ParasitesClaire Loiseau Carolina Chagas, Anonymous, Luz García-Longoria2023-08-11 14:14:56 View
23 Jan 2023
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Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense

Whole genome transcriptome reveals metabolic and immune susceptibility factors for Trypanosoma congolense infection in West-African livestock

Recommended by based on reviews by 2 anonymous reviewers

African trypanosomiasis is caused by to the infection of a protozoan parasite of the Trypanosoma genus. It is transmitted by the tsetse fly, and is largely affecting cattle in the sub-humid areas of Africa, causing a high economic impact. However, not all the bovine strains are equally susceptible to the infection (1). 

In order to dissect the mechanisms underlying susceptibility to African trypanosoma infection, Peylhard et al (2) performed blood transcriptional profiles of trypanotolerant, trypanosensitive and mixed cattle breeds, before and after experimental infection with T. congolense

First of all, the authors have characterized the basal transcriptional profiles in the blood of the different breeds under study, which could be classified in a wide array of functional pathways. Of note, after infection some pathways were consistently enriched in all the group tested. Among them, the immune system-related ones were again on the top functions reported. The search for specific canonical pathways pointed to a prominent role of lipid and cholesterol-related pathways, as well as mitochondrial function and B and T lymphocyte activation.

However, the analysis of infected animals demonstrated that trypanosusceptible animals showed a stronger transcriptomic reprogramming, highly enriched in specific metabolic and immunological pathways. It is worthy to highlight striking differences in genes involved in immune signal transduction, cytokines and markers of different leukocyte subpopulations.

This work represents undoubtedly a significant momentum in the field, since the authors explore in deep a wide panel of cattle breeds representing the majority of West-African taurine and zebu in a systematic way. Since the animals were studied at different timepoints after infection, future longitudinal analyses of these datasets will be providing a precious insight on the kinetics of immune and metabolic reprogramming associated with susceptibility and tolerance to African trypanosoma infection, widening the application of this interesting study into new therapeutic interventions.

References

1. Berthier D, Peylhard M, Dayo G-K, Flori L, Sylla S, Bolly S, Sakande H, Chantal I, Thevenon S (2015) A Comparison of Phenotypic Traits Related to Trypanotolerance in Five West African Cattle Breeds Highlights the Value of Shorthorn Taurine Breeds. PLOS ONE, 10, e0126498. https://doi.org/10.1371/journal.pone.0126498

2. Peylhard M, Berthier D, Dayo G-K, Chantal I, Sylla S, Nidelet S, Dubois E, Martin G, Sempéré G, Flori L, Thévenon S (2022) Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense. bioRxiv, 2022.06.10.495622, ver. 2 peer-reviewed and recommended by Peer Community Infections. https://doi.org/10.1101/2022.06.10.495622.

Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolenseMoana Peylhard, David Berthier, Guiguigbaza-Kossigan Dayo, Isabelle Chantal, Souleymane Sylla, Sabine Nidelet, Emeric Dubois, Guillaume Martin, Guilhem Sempéré, Laurence Flori, Sophie Thévenon<p>Animal African trypanosomosis, caused by blood protozoan parasites transmitted mainly by tsetse flies, represents a major constraint for millions of cattle in sub-Saharan Africa. Exposed cattle include trypanosusceptible indicine breeds, severe...Animal diseases, Genomics, functional genomics of hosts, infectious agents, or vectors, Resistance/Virulence/ToleranceConcepción MarañónAnonymous, Anonymous2022-06-14 17:06:57 View
23 Mar 2023
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The helper strategy in vector-transmission of plant viruses

The intriguing success of helper components in vector-transmission of plant viruses.

Recommended by based on reviews by Jamie Bojko and Olivier Schumpp

Most plant-infecting viruses rely on an animal vector to be transmitted from one sessile host plant to another. A fascinating aspect of virus-vector interactions is the fact that viruses from different clades produce different proteins to bind vector receptors (1). Two major processes are described. In the “capsid strategy”, a motif of the capsid protein is directly binding to the vector receptor. In the “helper strategy”, a non-structural component, the helper component (HC), establishes a bridge between the virus particle and the vector’s receptor.   

In this exhaustive review focusing on hemipteran insect vectors, Di Mattia et al. (2) are revisiting the helper strategy in light of recent results. The authors first place the discoveries of the HC strategy in a historical context, suggesting that HC are exclusively found in non-circulative viruses (viruses that only attach to the vector). They present an overview of the nature and modes of action of helper components in the major virus clades of non-circulative viruses (Potyviruses and Caulimoviruses). Authors then detail recent advances, to which they have significantly contributed, showing that the helper strategy also appears widespread in circulative transmission categories (Tenuiviruses, Nanoviruses). 

In an extensive perspective section, they raise the question of the evolutionary significance of the existence of HC in numerous unrelated viruses, transmitted by unrelated vectors through different mechanisms. They explore the hypothesis that the helper strategy evolved several times independently in distinct viral clades and for different reasons. In particular, they present several potential benefits of plant virus HC related to virus cooperation, collective transmission and effector-driven infectivity.

As pointed out by both reviewers, this is a very clear and synthetic review. Di Mattia et al. present an exhaustive overview of virus HC-vector molecular interactions and address functionally and evolutionarily important questions. This review should benefit a large audience interested in host-virus interactions and transmission processes.

REFERENCES

(1) Ng JCK, Falk BW (2006) Virus-Vector Interactions Mediating Nonpersistent and Semipersistent Transmission of Plant Viruses. Annual Review of Phytopathology, 44, 183–212. https://doi.org/10.1146/annurev.phyto.44.070505.143325

(2) Di Mattia J, Zeddam J-L, Uzest M, Blanc S (2023) The helper strategy in vector-transmission of plant viruses. Zenodo, ver. 2 peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.5281/zenodo.7709290

The helper strategy in vector-transmission of plant virusesDi Mattia Jérémy, Zeddam Jean Louis, Uzest Marilyne and Stéphane Blanc<p>An intriguing aspect of vector-transmission of plant viruses is the frequent involvement of a helper component (HC). HCs are virus-encoded non-structural proteins produced in infected plant cells that are mandatory for the transmission success....Evolution of hosts, infectious agents, or vectors, Interactions between hosts and infectious agents/vectors, Molecular biology of infections, Molecular genetics of hosts, infectious agents, or vectors, Plant diseases, Vectors, VirusesChristine Coustau2022-10-28 17:32:39 View
21 Sep 2023
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Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potential

Fill in one gap in our understanding of CHIKV intra-vector dynamics

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

Mosquitoes are first vector of pathogen worldwide and transmit several arbovirus, most of them leading to major outbreaks (1). Chikungunya virus (CHIKV) is a perfect example of the “explosive type” of arbovirus, as observed in La Réunion Island in 2005-2006 (2-6) and also in the outbreak of 2007 in Italy (7), both vectorized by Ae. albopictus. Being able to better understand CHIKV intra-vector dynamics is still of major interest since not all chikungunya strain are explosive ones (8). 

In this study (9), the authors have evaluated the vector competence of a local strain of Aedes albopictus (collected in Lyon, France) for CHIKV. They evaluated infection, dissemination and transmission dynamics of CHIKV using different dose of virus in individual mosquitoes from day 2 to day 20 post exposure, by titration and quantification of CHIKV RNA load in the saliva. As highlighted by both reviewers, the most innovative idea in this study was the use of three different oral doses trying to span human viraemia detected in two published studies (10-11), doses that were estimated through their model of human CHIKV viremia in the blood.  They have found that CHIKV dissemination from the Ae. albopictus midgut depends on the interaction between time post-exposure and virus dose (already highlighted by other international publications).  Then their results were implemented in the agent-based model nosoi to estimate the epidemic potential of CHIKV in a French population of Ae. albopictus, using realistic vectorial capacity parameters.

To conclude, the authors have discussed the importance of other parameters that could influence vector competence as mosquito microbiota and temperature, parameters that need also to be estimated in local mosquito population to improve the risk assessment through modelling.  

As pointed out by both reviewers, this is a nice study, well written and easy to read. These results allow filling in another gap of our understanding of CHIKV intra-vector dynamics and highlight the epidemic potential of CHIKV upon transmission by Aedes albopictus in mainland France. For all these reasons, I chose to recommend this article for Peer Community In Infections.

References

1.       Marine Viglietta, Rachel Bellone, Adrien Albert Blisnick, Anna-Bella Failloux. (2021). Vector Specificity of Arbovirus Transmission. Front Microbiol Dec 9;12:773211. https://doi.org/10.3389/fmicb.2021.773211

2.       Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney M-C, Lavenir R, Pardigon N, Reynes J-M, Pettinelli F, Biscornet L, Diancourt L, Michel S, Duquerroy S, Guigon G, Frenkiel M-P, Bréhin A-C, Cubito N, Desprès P, Kunst F, Rey FA, Zeller H, Brisse S. (2006). Genome Microevolution of Chikungunya viruses Causing the Indian Ocean Outbreak. 2006. PLoS Medicine, 3, e263. https://doi.org/10.1371/journal.pmed.0030263

3.       Bonilauri P, Bellini R, Calzolari M, Angelini R, Venturi L, Fallacara F, Cordioli P, 687 Angelini P, Venturelli C, Merialdi G, Dottori M. (2008). Chikungunya Virus in Aedes albopictus, Italy. Emerging Infectious 689 Diseases, 14, 852–854. https://doi.org/10.3201/eid1405.071144

4.       Pagès F, Peyrefitte CN, Mve MT, Jarjaval F, Brisse S, Iteman I, Gravier P, Tolou H, Nkoghe D, Grandadam M. (2009). Aedes albopictus Mosquito: The Main Vector of the 2007 Chikungunya Outbreak in Gabon. PLoS ONE, 4, e4691. https://doi.org/10.1371/journal.pone.0004691

5.       Paupy C, Kassa FK, Caron M, Nkoghé D, Leroy EM (2012) A Chikungunya Outbreak Associated with the Vector Aedes albopictus in Remote Villages of Gabon. Vector-Borne and Zoonotic Diseases, 12, 167–169. https://doi.org/10.1089/vbz.2011.0736

6.       Mombouli J-V, Bitsindou P, Elion DOA, Grolla A, Feldmann H, Niama FR, Parra H-J, Munster VJ. (2013). Chikungunya Virus Infection, Brazzaville, Republic of Congo, 2011. Emerging Infectious Diseases, 19, 1542–1543. https://doi.org/10.3201/eid1909.130451

7.       Venturi G, Luca MD, Fortuna C, Remoli ME, Riccardo F, Severini F, Toma L, Manso MD, Benedetti E, Caporali MG, Amendola A, Fiorentini C, Liberato CD, Giammattei R, Romi R, Pezzotti P, Rezza G, Rizzo C. (2017). Detection of a chikungunya outbreak in Central Italy, August to September 2017. Eurosurveillance, 22, 17–00646. https://doi.org/10.2807/1560-7917.es.2017.22.39.17-00646

8.       de Lima Cavalcanti, T.Y.V.; Pereira, M.R.; de Paula, S.O.; Franca, R.F.d.O. (2022). A Review on Chikungunya Virus Epidemiology, Pathogenesis and Current Vaccine Development. Viruses 2022, 14, 969. https://doi.org/10.3390/v14050969

9.       Barbara Viginier, Lucie Cappuccio, Celine Garnier, Edwige Martin, Carine Maisse, Claire Valiente Moro, Guillaume Minard, Albin Fontaine, Sebastian Lequime, Maxime Ratinier, Frederick Arnaud, Vincent Raquin. (2023). Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potential. medRxiv, ver.3, peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2022.11.06.22281997

10.     Appassakij H, Khuntikij P, Kemapunmanus M, Wutthanarungsan R, Silpapojakul K (2013) Viremic profiles in CHIKV-infected cases. Transfusion, 53, 2567–2574. https://doi.org/10.1111/j.1537-2995.2012.03960.x

11.     Riswari SF, Ma’roef CN, Djauhari H, Kosasih H, Perkasa A, Yudhaputri FA, Artika IM, Williams M, Ven A van der, Myint KS, Alisjahbana B, Ledermann JP, Powers AM, Jaya UA (2015) Study of viremic profile in febrile specimens of chikungunya in Bandung, Indonesia. Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology, 74, 61–5. https://doi.org/10.1016/j.jcv.2015.11.017

Chikungunya intra-vector dynamics in *Aedes albopictus* from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier permissiveness and supports local epidemic potentialBarbara Viginier, Lucie Cappuccio, Celine Garnier, Edwige Martin, Carine Maisse, Claire Valiente Moro, Guillaume Minard, Albin Fontaine, Sebastian Lequime, Maxime Ratinier, Frederick Arnaud, Vincent Raquin<p>Arbovirus emergence and epidemic potential, as approximated by the vectorial capacity formula, depends on host and vector parameters, including the vector intrinsic ability to replicate then transmit the pathogen known as vector competence. Vec...Epidemiology, Vectors, VirusesSara Moutailler2023-06-17 15:59:17 View
03 Nov 2023
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Longitudinal Survey of Astrovirus infection in different bat species in Zimbabwe: Evidence of high genetic Astrovirus diversity

High diversity and evidence for inter-species transmission in astroviruses surveyed from bats in Zibabwae

Recommended by based on reviews by 2 anonymous reviewers

Most infectious diseases of humans are zoonoses, and many of these come from particularly species diverse reservoir taxa, such as bats, birds, and rodents (1). Because of our changing landscape, there is increased exposure of humans to wildlife diseases reservoirs, yet we have little basic information about prevalence, hotspots, and transmission factors of most zoonotic pathogens. Viruses are particularly worrisome as a public health risk due to their fast mutation rates and well-known cross-species transmission abilities. There is a global push to better survey wildlife for viruses (2), but these studies are difficult, and the problem is vast. Astroviruses (AstVs) comprise a diverse family of ssRNA viruses known from mammals and birds. Astroviruses can cause gastroenteritis in humans and are more common in elderly and young children, but the relationship of human to non-human Astroviridae as well as transmission routes are unclear.  AstVs have been detected at high prevalence in bats in multiple studies (3,4), but it is unclear what factors, such as co-infecting viruses and bat reproductive phenology, influence viral shedding and prevalence.
In this recommended study, Vimbiso et al. (5) study the prevalence and diversity of astroviruses in different insectivorous and frugivorous chiropteran species roosting in trees, caves and building basements across Zimbabwe, a region never investigated for astroviruses. Using both pooled population samples and individual samples from 11 different sites, the authors screened for astrovirus prevalence via RT-PCR and identified bat taxa using mitochondrial gene sequencing. An overall prevalence of 10-14% infection was recorded. No clear association of increased astrovirus and coronavirus coinfection was detected, and although astrovirus infection varied over the season, it did not do so in consistent ways across the two primary sampling sites, Magweto and Chirundu. A phylogeny generated by sequencing all of the astrovirus positive samples showed evidence that most of the viral lineages are transmitting within species but across Zibabwae such that most phylogenetic lineages grouped viruses from the same host species together. However, there was ample evidence for interspecies transmission between bats. Finally, a small percentage of the total astrovirus diversity from Zibabwae clustered with sequences from humans. The timing and direction of the transmission between humans and bats need further investigation.
 
This study provides important baseline data about viral diversity and does an excellent job of capturing the spatial, temporal, host species, and sequence level dynamics of the astroviruses. There are clear limitations on how this study can be interpreted due to different sampling regimes and, in particular, the fact that each of the two primary sites was only explored for temporal variation over a single calendar year. That said, the grand diversity of astroviruses demonstrated in insectivorous bats in Zibabwae shows that we are only seeing the very tip of the iceberg with respect to viral diversity with zoonotic potential. As suggested by the reviewers, more studies like this are needed to understand the basic ecology of viruses and to aid in predicting epidemics.

References

1. Mollentze N, Streicker DG. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proceedings of the National Academy of Sciences. 2020 Apr 28;117(17):9423-30. https://doi.org/10.1073/pnas.1919176117
2. Carroll D, Daszak P, Wolfe ND, Gao GF, Morel CM, Morzaria S, et al. The Global Virome Project. Science. 2018 Feb 23;359(6378):872-4. https://doi.org/10.1126/science.aap7463
3. Lee SY, Son KD, Yong-Sik K, Wang SJ, Kim YK, Jheong WH, et al. Genetic diversity and phylogenetic analysis of newly discovered bat astroviruses in Korea. Arch Virol. 2018;163(11):3065-72. https://doi.org/10.1007/s00705-018-3992-6
4. Seltmann A, Corman VM, Rasche A, Drosten C, Czirják GÁ, Bernard H, et al. Seasonal Fluctuations of Astrovirus, But Not Coronavirus Shedding in Bats Inhabiting Human-Modified Tropical Forests. EcoHealth. 2017 Jun 1;14(2):272-84. https://doi.org/10.1007/s10393-017-1245-x
5. Vimbiso C, Hélène DN, Malika A, Getrude M, Valérie P, Ngoni C, et al. Longitudinal Survey of Astrovirus infection in different bat species in Zimbabwe: Evidence of high genetic Astrovirus diversity. bioRxiv, 2023.04.14.536987, ver. 6 peer-reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.04.14.536987

Longitudinal Survey of Astrovirus infection in different bat species in Zimbabwe: Evidence of high genetic Astrovirus diversityVimbiso Chidoti, Helene De Nys, Malika Abdi, Getrudre Mashura, Valerie Pinarello, Ngoni Chiweshe, Gift Matope, Laure Guerrini, Davies Pfulenyi, Julien Cappelle, Ellen Mwandiringana, Dorothee Misse, Gori Elizabeth, Mathieu Bourgarel, Florian Liegeois<p>Astroviruses (AstVs) have been discovered in over 80 animal species including diverse bat species and avian species. A study on Astrovirus circulation and diversity in different insectivorous and frugivorous chiropteran species roosting in tree...Animal diseases, Epidemiology, Molecular genetics of hosts, infectious agents, or vectors, Reservoirs, Viruses, ZoonosesTim James2023-04-18 14:58:43 View
07 Feb 2023
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Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populations

Unveiling the complex interactions between members of gut microbiomes: a significant advance provided by an exhaustive study of wild bank voles

Recommended by based on reviews by Jason Anders and 1 anonymous reviewer

The gut of vertebrates is a host for hundreds or thousands of different species of microorganisms named the gut microbiome. This latter may differ greatly in natural environments between individuals, populations and species (1). The vertebrate gut microbiome plays key roles in host fitness through functions including nutrient acquisition, immunity and defense against infectious agents. While bank voles are small mammals potentially reservoirs of a large number of infectious agents, questions about the links between their gut microbiome and the presence of pathogens are scarcely addressed. 

In this study, Bouilloud et al. (2) used complementary analyses of community and microbial ecology to (i) assess the variability of gut bacteriome diversity and composition in wild populations of the bank vole Myodes glareolus collected in four different sites in Eastern France and (ii) evaluate the three-way interactions between the gut bacteriota, the gastro-intestinal helminths and pathogenic bacteria detected in the spleen. Authors identified important variations of the gut bacteriota composition and diversity among bank voles mainly explained by sampling localities. They found positive correlations between the specific richness of both the gut bacteria and the helminth community, as well as between the composition of these two communities, even when accounting for the influence of geographical distance. The helminths Aonchotheca murissylvatici, Heligmosomum mixtum and the bacteria Bartonella sp were the main taxa associated with the whole gut bacteria composition. Besides, changes in relative abundance of particular gut bacterial taxa were specifically associated with other helminths (Mastophorus muris, Catenotaenia henttoneni, Paranoplocephala omphalodes and Trichuris arvicolae) or pathogenic bacteria. Infections with Neoehrlichia mikurensis, Orientia sp, Rickettsia sp and P. omphalodes were especially associated with lower relative abundance of members of the family Erysipelotrichaceae (Firmicutes), while coinfections with higher number of bacterial infections were associated with lower relative abundance of members of the Bacteroidales family (Bacteroidetes). 

As pointed out by both reviewers, this study represents a significant advance in the field. I would like to commend the authors for this enormous work. The amount of data, analyses and results is considerable which has sometimes complicated the understanding of the story at the beginning of the evaluation process. Thanks to constructive scientific interactions with both reviewers through the two rounds of evaluation, the authors have efficiently addressed the reviewer's concerns and improved the manuscript, making this great story easier to read. The innovative results of this study emphasize the complex interlinkages between gut bacteriome and infections in wild animal populations and I strongly recommend this article for publication In Peer Community Infections. 

References

(1) Vujkovic-Cvijin I, Sklar J, Jiang L, Natarajan L, Knight R, Belkaid Y (2020) Host variables confound gut microbiota studies of human disease. Nature, 587, 448–454. https://doi.org/10.1038/s41586-020-2881-9

(2) Bouilloud M, Galan M, Dubois A, Diagne C, Marianneau P, Roche B, Charbonnel N (2023) Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populations. biorxiv, 2022.05.23.493084, ver. 2 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.05.23.493084

Three-way relationships between gut microbiota, helminth assemblages and bacterial infections in wild rodent populationsMarie Bouilloud, Maxime Galan, Adelaide Dubois, Christophe Diagne, Philippe Marianneau, Benjamin Roche, Nathalie Charbonnel<p>Background</p> <p>Despite its central role in host fitness, the gut microbiota may differ greatly between individuals. This variability is often mediated by environmental or host factors such as diet, genetics, and infections. Recently, a part...Disease Ecology/Evolution, Ecohealth, Interactions between hosts and infectious agents/vectors, Reservoirs, ZoonosesThomas Pollet2022-05-25 10:13:23 View
14 Nov 2022
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Ehrlichia ruminantium uses its transmembrane protein Ape to adhere to host bovine aortic endothelial cells

Adhesion process of Ehrlichia ruminantium to its host cell: the role of the protein ERGACDS01230 elucidated

Recommended by based on reviews by Rodolfo García-Contreras and Alejandro Cabezas-Cruz

As recently reported by the world organisation for animal health, 60% of infectious diseases are zoonotic with a significant part associated to ticks. Ticks can transmit various pathogens such as bacteria, viruses and parasites. Among pathogens known to be transmitted by ticks, Ehrlichia ruminantium is an obligate intracellular Gram-negative bacterium responsible for the fatal heartwater disease of domestic and wild ruminants (Allsopp, 2010). E. ruminantium is transmitted by ticks of the genus Amblyomma in the tropical and sub-Saharan areas, as well as in the Caribbean islands. It constitutes a major threat for the American livestock industries since a suitable tick vector is already present in the American mainland and potential introduction of infected A. variegatum through migratory birds or uncontrolled movement of animals from Caribbean could occur (i.e. Deem, 1998 ; Kasari et al 2010). The disease is also a major obstacle to the introduction of animals from heartwater-free to heartwater-infected areas into sub-Saharan Africa and thus restrains breeding programs aiming at upgrading local stocks (Allsopp, 2010).

In this context, it is essential to develop control strategies against heartwater, as developing effective vaccines, for instance. Such an objective requires a better understanding of the early interaction of E. ruminantium and its host cells and of the mechanisms associated with bacterial adhesion to the host-cell. In this study, the authors. studied the role of E. ruminantium membrane protein ERGA_CDS_01230 in the adhesion process to host bovine aortic endothelial cells (BAEC).

After successfully producing the recombinant version of the protein, Pinarello et al (2022) followed the in vitro culture of E. ruminantium in BAEC and observed that the expression of the protein peaked at the extracellular infectious elementary body stages. This result would suggest the likely involvement of the protein in the early interaction of E. ruminantium with its host cells. The authors then showed using flow cytometry, and scanning electron microscopy, that beads coated with the recombinant protein adhered to BAEC. In addition, they also observed that the adhesion protein of E. ruminantium interacted with proteins of the cell's lysate, membrane and organelle fractions. Additionally, enzymatic treatment, degrading dermatan and chondroitin sulfates on the surface of BAEC, was associated with a 50% reduction in the number of bacteria in the host cell after a development cycle, indicating that glycosaminoglycans might play a role in the adhesion of E. ruminantium to the host-cell. Finally, the authors observed that the adhesion protein of E. ruminantium induced a humoral response in vaccinated animals, making this protein a possible vaccine candidate.

As rightly pointed out by both reviewers, the results of this study represent a significant advance (i) in the understanding of the role of the E. ruminantium membrane protein ERGA_CDS_01230 in the adhesion process to the host-cell and (ii) in the development of new control strategies against heartwater as this protein might potentially be used as an immunogen for the development of future vaccines.

References

Allsopp, B.A. (2010). Natural history of Ehrlichia ruminantium. Vet Parasitol 167, 123-135. https://doi.org/10.1016/j.vetpar.2009.09.014

Deem, S.L. (1998). A review of heartwater and the threat of introduction of Cowdria ruminantium and Amblyomma spp. ticks to the American mainland. J Zoo Wildl Med 29, 109-113.

Kasari, T.R. et al (2010). Recognition of the threat of Ehrlichia ruminantium infection in domestic and wild ruminants in the continental United States. J Am Vet Med Assoc. 237:520-30. https://doi.org/10.2460/javma.237.5.520

Pinarello V, Bencurova E, Marcelino I, Gros O, Puech C, Bhide M, Vachiery N, Meyer DF (2022) Ehrlichia ruminantium uses its transmembrane protein Ape to adhere to host bovine aortic endothelial cells. bioRxiv, 2021.06.15.447525, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2021.06.15.447525

*Ehrlichia ruminantium* uses its transmembrane protein Ape to adhere to host bovine aortic endothelial cellsValérie Pinarello, Elena Bencurova, Isabel Marcelino, Olivier Gros, Carinne Puech, Mangesh Bhide, Nathalie Vachiery, Damien F. Meyer<p><em>Ehrlichia ruminantium</em> is an obligate intracellular bacterium, transmitted by ticks of the genus <em>Amblyomma</em> and responsible for heartwater, a disease of domestic and wild ruminants. High genetic diversity of <em>E. ruminantium</...Interactions between hosts and infectious agents/vectors, Microbiology of infectionsThomas Pollet Rodolfo García-Contreras, Alejandro Cabezas-Cruz2021-10-14 16:54:54 View
28 Oct 2022
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Development of nine microsatellite loci for Trypanosoma lewisi, a potential human pathogen in Western Africa and South-East Asia, and preliminary population genetics analyses

Preliminary population genetic analysis of Trypanosoma lewisi

Recommended by based on reviews by Gabriele Schönian and 1 anonymous reviewer

Trypanosoma lewisi is an atypical trypanosome species. Transmitted by fleas, it has a high prevalence and worldwide distribution in small mammals, especially rats [1]. Although not typically thought to infect humans, there has been a number of reports of human infections by T. lewisi in Asia including a case of a fatal infection in an infant [2]. The fact that the parasite is resistant to lysis by normal human serum [3] suggests that many people, especially immunocompromised individuals, may be at risk from zoonotic infections by this pathogen, particularly in regions where there is close contact with T. lewisi-infected rat fleas. Indeed, it is also possible that cryptic T. lewisi infections exist but have hitherto gone undetected. Such asymptomatic infections have been detected for a number of parasitic infections including the related parasite T. b. gambiense [4]. 
 
Despite the fact that T. lewisi parasites pose a risk to human health, very little is known about their population structure, reproductive mode, population size or dispersal. In the article [5], Ségard et al. presented the first attempt at examining the population structure of the parasite. They developed microsatellite markers and used them to analyse a small set of samples from West Africa and Southeast Asia. Although the number of microsatellite markers is not very high and they encountered problems of PCR amplification especially of the southeast Asian samples, they did provide preliminary data that hints at a clonal population structure with rare recombination and suggests population subdivisions occurring at a scale that is equal, and probably smaller than a neighborhood of several houses with a short generation time. These are very interesting preliminary findings that will need to be validated using a larger cohort with more markers or by whole genome sequencing.
 

References


[1] Hoare CA (1972) The trypanosomes of mammals. A zoological monograph. The trypanosomes of mammals. A zoological monograph.

[2] Truc P, Büscher P, Cuny G, Gonzatti MI, Jannin J, Joshi P, Juyal P, Lun Z-R, Mattioli R, Pays E, Simarro PP, Teixeira MMG, Touratier L, Vincendeau P, Desquesnes M (2013) Atypical Human Infections by Animal Trypanosomes. PLOS Neglected Tropical Diseases, 7, e2256. https://doi.org/10.1371/journal.pntd.0002256

[3] Lun Z-R, Wen Y-Z, Uzureau P, Lecordier L, Lai D-H, Lan Y-G, Desquesnes M, Geng G-Q, Yang T-B, Zhou W-L, Jannin JG, Simarro PP, Truc P, Vincendeau P, Pays E (2015) Resistance to normal human serum reveals Trypanosoma lewisi as an underestimated human pathogen. Molecular and Biochemical Parasitology, 199, 58–61. https://doi.org/10.1016/j.molbiopara.2015.03.007

[4] Büscher P, Bart J-M, Boelaert M, Bucheton B, Cecchi G, Chitnis N, Courtin D, Figueiredo LM, Franco J-R, Grébaut P, Hasker E, Ilboudo H, Jamonneau V, Koffi M, Lejon V, MacLeod A, Masumu J, Matovu E, Mattioli R, Noyes H, Picado A, Rock KS, Rotureau B, Simo G, Thévenon S, Trindade S, Truc P, Reet NV (2018) Do Cryptic Reservoirs Threaten Gambiense-Sleeping Sickness Elimination? Trends in Parasitology, 34, 197–207. https://doi.org/10.1016/j.pt.2017.11.008

[5] Ségard A, Roméro A, Ravel S, Truc P, Gauthier D, Gauthier P, Dossou H-J, Sylvestre B, Houéménou G, Morand S, Chaisiri K, Noûs C, De Meeûs T (2022) Development of nine microsatellite loci for Trypanosoma lewisi, a potential human pathogen in Western Africa and South-East Asia, and preliminary population genetics analyses. Zenodo, 6460010, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6460010

Development of nine microsatellite loci for Trypanosoma lewisi, a potential human pathogen in Western Africa and South-East Asia, and preliminary population genetics analysesAdeline Ségard, Audrey Romero, Sophie Ravel, Philippe Truc, Gauthier Dobigny, Philippe Gauthier, Jonas Etougbetche, Henri-Joel Dossou, Sylvestre Badou, Gualbert Houéménou, Serge Morand, Kittipong Chaisiri, Camille Noûs, Thierry deMeeûs<p><em>Trypanosoma lewisi</em> belongs to the so-called atypical trypanosomes that occasionally affect humans. It shares the same hosts and flea vector of other medically relevant pathogenic agents as Yersinia pestis, the agent of plague. Increasi...Animal diseases, Disease Ecology/Evolution, Ecology of hosts, infectious agents, or vectors, Eukaryotic pathogens/symbionts, Evolution of hosts, infectious agents, or vectors, Microbiology of infections, Parasites, Population genetics of hosts, in...Annette MacLeod2022-04-21 17:04:37 View
28 May 2024
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HIV self-testing positivity rate and linkage to confirmatory testing and care: a telephone survey in Côte d'Ivoire, Mali and Senegal

The benefits of HIV self-testing in West Africa: quantified.

Recommended by ORCID_LOGO based on reviews by 3 anonymous reviewers

Despite decades of advances and understanding of the indiscriminate nature of human immunodeficiency virus (HIV), it remains shrouded in stigma that makes it difficult to reach some key populations at risk of transmission. The advent of self-testing technology for HIV (HIVST) has opened much-needed potential for bringing privacy to prevention that is crucial for curtailing its continued spread (Johnson et al., 2014). The HIV Self-Testing in Africa (STAR) Initiative (https://www.psi.org/fr/project/star/), carried out in Eastern and Southern Africa between 2015 and 2020 (Simwinga et al., 2022), demonstrated the market and public health operational potential of HIVST of different distribution methods. From 2019 to 2022, the “AutoTest de dépistage du VIH : Libre d’Accéder à la connaissance de son Statut" (ATLAS, translating to “HIVST: Freedom to know your status”) program built on these findings to quantify the public health value of HIVST for reaching key populations in West Africa (specifically, Mali, Senegal and Côte d’Ivoire) (Ky-Zerbo et al., 2022).

The innovative secondary distribution methods these studies employed, where the primary targeted populations were also encouraged to take and provide tests to their contacts, helped widen the reach of HIVST within key population networks beyond those relying on access to HIV testing facilities.

 

The tricky part of the self-testing model lies in assessing its reach and impact while maintaining the privacy of self-testers that is central to its success. Following voluntary phone survey methods that previously were able to show expanded reach of HIVST to first-time testers in key populations in West Africa and high rates of confirmatory testing and treatment seeking (Kra et al., 2022), Kra et al. (Kra et al., 2024) quantified how many of these self-tests led to a positive result – allowing wider assessment of follow-up behaviors and positivity rates among the hard-to-reach populations the program had targeted. 

 

While the numbers were low, the results were informative. Among respondents who reported a positive (“reactive”) HIVST, just 44% proceeded to confirmatory testing. This is lower than in other populations where HIVST follow-up has been assessed (Thirumurthy et al., 2016). The main reasons given for not confirming a reactive self-test was misinterpretation of HIVST results and not understanding that confirmatory testing was needed. The result thus highlighted a need for improved communication on how to correctly interpret HIVST results, and the authors provided ranges for how this misinterpretation could have affected their positivity estimates. However, the majority of those who sought confirmatory testing did so within 3 months, and nearly all of those with confirmed infection started on treatment. HIV positivity rates in the three countries were all higher than other published HIV positivity estimates (Giguère et al., 2021; Maheu-Giroux et al., 2019), suggesting that HIVST methods were highly effective at reaching the targeted communities. 

Finally, while the authors demonstrated their methods as an effective way of assessing the utility of HIVST campaigns and identifying ways to improve them, the follow-up surveys are likely too costly to replace current passive surveillance methods for assessing community disease burden. That said, these precious data should be taken as validation of the public health value of HIV self-testing in key populations across communities in West Africa. With improvements in communicating instructions for use and follow-up, there is little doubt that the innovation of HIVST primary and secondary distribution could become a widely useful addition to the fight against HIV. 

 

References

Giguère, K., Eaton, J. W., Marsh, K., Johnson, L. F., Johnson, C. C., Ehui, E., Jahn, A., Wanyeki, I., Mbofana, F., Bakiono, F., Mahy, M., & Maheu-Giroux, M. (2021). Trends in knowledge of HIV status and efficiency of HIV testing services in sub-Saharan Africa, 2000–20: a modelling study using survey and HIV testing programme data. The Lancet HIV, 8(5), e284–e293. https://doi.org/10.1016/S2352-3018(20)30315-5

Johnson, C., Baggaley, R., Forsythe, S., Van Rooyen, H., Ford, N., Napierala Mavedzenge, S., Corbett, E., Natarajan, P., & Taegtmeyer, M. (2014). Realizing the potential for HIV self-testing. In AIDS and Behavior (Vol. 18, Issue SUPPL. 4). Springer New York LLC. https://doi.org/10.1007/s10461-014-0832-x

Kra, A. K., Fosto, A. S., N’guessan, K. N., Geoffroy, O., Younoussa, S., Kabemba, O. K., Gueye, P. A., Ndeye, P. D., Rouveau, N., Boily, M. C., Silhol, R., d’Elbée, M., Maheu-Giroux, M., Vautier, A., & Larmarange, J. (2022). Can HIV self-testing reach first-time testers? A telephone survey among self-test end users in Côte d’Ivoire, Mali, and Senegal. BMC Infectious Diseases, 22. https://doi.org/10.1186/s12879-023-08626-w

Kra, A. K., Fotso, A. S., Rouveau, N., Maheu-Giroux, M., Boily, M.-C., Silhol, R., d’Elbée, M., Vautier, A., Lamarange, J., & the Atlas team. (2024). HIV self-testing positivity rate and linkage to confirmatory testing and care: a telephone survey in Côte d’Ivoire, Mali, and Senegal. MedRxiv, Ver. 4 Peer-Reviewed and Recommended by Peer Community in Infections, 2023.06.10.23291206. https://doi.org/https://doi.org/10.1101/2023.06.10.23291206

Ky-Zerbo, O., Desclaux, A., Boye, S., Maheu-Giroux, M., Rouveau, N., Vautier, A., Camara, C. S., Kouadio, B. A., Sow, S., Doumenc-Aidara, C., Gueye, P. A., Geoffroy, O., Kamemba, O. K., Ehui, E., Ndour, C. T., Keita, A., & Larmarange, J. (2022). “I take it and give it to my partners who will give it to their partners”: Secondary distribution of HIV self-tests by key populations in Côte d’Ivoire, Mali, and Senegal. BMC Infectious Diseases, 22. https://doi.org/10.1186/s12879-023-08319-4

Maheu-Giroux, M., Marsh, K., Doyle, C. M., Godin, A., Lanièce Delaunay, C., Johnson, L. F., Jahn, A., Abo, K., Mbofana, F., Boily, M. C., Buckeridge, D. L., Hankins, C. A., & Eaton, J. W. (2019). National HIV testing and diagnosis coverage in sub-Saharan Africa: A new modeling tool for estimating the “first 90” from program and survey data. AIDS, 33, S255–S269. https://doi.org/10.1097/QAD.0000000000002386

Simwinga, M., Gwanu, L., Hensen, B., Sigande, L., Mainga, M., Phiri, T., Mwanza, E., Kabumbu, M., Mulubwa, C., Mwenge, L., Bwalya, C., Kumwenda, M., Mubanga, E., Mee, P., Johnson, C. C., Corbett, E. L., Hatzold, K., Neuman, M., Ayles, H., & Taegtmeyer, M. (2022). Lessons learned from implementation of four HIV self-testing (HIVST) distribution models in Zambia: applying the Consolidated Framework for Implementation Research to understand impact of contextual factors on implementation. BMC Infectious Diseases, 22(Suppl 1). https://doi.org/10.1186/s12879-024-09168-5

Thirumurthy, H., Masters, S. H., Mavedzenge, S. N., Maman, S., Omanga, E., & Agot, K. (2016). Promoting male partner HIV testing and safer sexual decision making through secondary distribution of self-tests by HIV-negative female sex workers and women receiving antenatal and post-partum care in Kenya: a cohort study. The Lancet HIV, 3(6), e266–e274. https://doi.org/10.1016/S2352-3018(16)00041-2

 

HIV self-testing positivity rate and linkage to confirmatory testing and care: a telephone survey in Côte d'Ivoire, Mali and SenegalKra Djuhe Arsene Kouassi, Arlette Simo Fotso, Nicolas Rouveau, Mathieu Maheu-Giroux, Marie-Claude Boily, Romain Silhol, Marc d'Elbee, Anthony Vautier, Joseph Larmarange, ATLAS Team<p>HIV self-testing (HIVST) empowers individuals to decide when and where to test and with whom to share their results. From 2019 to 2022, the ATLAS program distributed ~ 400 000 HIVST kits in Côte d’Ivoire, Mali, and Senegal. It prioritised key p...EpidemiologyJessie Abbate2023-06-16 16:40:51 View