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19 Feb 2024
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Population genetics of Glossina palpalis gambiensis in the sleeping sickness focus of Boffa (Guinea) before and after eight years of vector control: no effect of control despite a significant decrease of human exposure to the disease

Reaching the last miles for transmission interruption of sleeping sickness in Guinea: follow-up of achievements and policy making using microsatellites-based population genetics

Recommended by ORCID_LOGO based on reviews by Fabien HALKETT and 2 anonymous reviewers

Thanks to the coordinated and sustained efforts of national control programs, the World Health Organization (WHO), bilateral cooperation and nongovernmental organizations, the incidence of Human African Trypanosomiasis (HAT), better known as sleeping sickness, has drastically decreased during the last two decades (WHO, 2023a). Indeed, between 1999 and 2022, the reported number of new cases of the chronic form of sleeping sickness (Trypanosoma brucei gambiense) fell by 97% (from 27 862 to 799), and the number of newly reported cases of the acute form of HAT (Trypanosoma brucei rhodesiense) fell by 94% (from 619 to 38) (WHO, 2023b). These encouraging trends led the WHO to target this debilitating and highly fatal (if untreated) vector-borne parasitic disease for elimination as a public health problem by 2020, and for interruption of transmission (zero case) by 2030 (WHO, 2021, WHO, 2023a). However, the disease is persisting in many foci, and even some cases of resurgence have been documented after unfortunate events such as war or pandemics (Moore et al., 1999; Sah et al., 2023. Simarro et al). Although effective control measures, diagnosis and treatment are complex and require specific skills (WHO, 2023), especially in a context which animal reservoirs, including hidden reservoirs, can contribute to the maintenance/persistence of infection (Welburn and Maudlin, 2012; Camara et al., 2021). Vector control therefore appears as a viable alternative to accelerate sleeping sickness transmission interruption, and WHO has identified some critical actions for HAT elimination, including the coordination of vector control and animal trypanosomiasis management among countries, stakeholders and other sectors (e.g. tourism and wildlife) through multisectoral national bodies to maximize synergies (WHO, 2021).

The paper by Kagbadouno and Collaborators (2024) uses microsatellite markers genotyping and population genetics tools to investigate the impact of 11 years of tiny target-based vector control on the population biology of Glossina palpalis gambiensis in Boffa, one of the three active sleeping sickness foci in Guinea (Kagbadouno et al., 2012). Although vector control significantly reduced the apparent densities of tsetse flies (and therefore the human exposure to the vector) as well as the prevalence and incidence of the disease in the Boffa HAT focus (Courtin et al., 2015), no genetic signature of vector control was observed as no difference in population size, before and after the onset of the control policy, was found. The authors then provided national programs and implementing partners with indications on the actions to be taken to (i) maintain the achievements of vector control (thus avoiding rebound/resurgence as was experienced in the past (Franco et al., 2014), and (ii) accelerate the momentum towards elimination by for example combining these vector control efforts with medical surveys for case detection and treatment, in line with WHO recommendations (WHO, 2021). 

References

Camara M, Soumah AM, Ilboudo H, Travaillé C, Clucas C, Cooper A, Kuispond Swar NR, Camara O, Sadissou I, Calvo Alvarez E, Crouzols A, Bart JM, Jamonneau V, Camara M, MacLeod A, Bucheton B, Rotureau B. Extravascular Dermal Trypanosomes in Suspected and Confirmed Cases of gambiense Human African Trypanosomiasis. Clin Infect Dis. 2021 Jul 1;73(1):12-20. https://doi.org/10.1093/cid/ciaa897

Courtin F, Camara M, Rayaisse JB, Kagbadouno M, Dama E, Camara O, Traore IS, Rouamba J, Peylhard M, Somda MB, Leno M, Lehane MJ, Torr SJ, Solano P, Jamonneau V, Bucheton B (2015) Reducing human-tsetse contact significantly enhances the efficacy of sleeping sickness active screening campaigns: a promising result in the context of elimination. PLoS Neglected Tropical Diseases, 9. https://doi.org/10.1371/journal.pntd.0003727

Franco JR, Simarro PP, Diarra A, Jannin JG. (2014) Epidemiology of human African trypanosomiasis. Clin Epidemiol. 6:257-75. https://doi.org/10.2147/CLEP.S39728

Kagbadouno, M. S., Séré, M., Ségard, A., Camara, A. D., Camara, M., Bucheton, B., ... & Ravel, S. (2023). Population genetics of Glossina palpalis gambiensis in the sleeping sickness focus of Boffa (Guinea) before and after eight years of vector control: no effect of control despite a significant decrease of human exposure to the disease. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2023.07.25.550445

Kagbadouno MS, Camara M, Rouamba J, Rayaisse JB, Traoré IS, Camara O, Onikoyamou MF, Courtin F, Ravel S, De Meeûs T, Bucheton B, Jamonneau V, Solano P (2012) Epidemiology of sleeping sickness in boffa (Guinea): where are the trypanosomes? PLoS Neglected Tropical Diseases, 6, e1949. https://doi.org/10.1371/journal.pntd.0001949 

Moore A, Richer M, Enrile M, Losio E, Roberts J, Levy D. Resurgence of sleeping sickness in Tambura County, Sudan. Am J Trop Med Hyg. 1999 Aug;61(2):315-8. https://doi.org/10.4269/ajtmh.1999.61.315

Sah R, Mohanty A, Rohilla R, Padhi BK. A resurgence of Sleeping sickness amidst the COVID-19 pandemic: Correspondence. Int J Surg Open. 2023 Apr;53:100604. https://doi.org/10.1016/j.ijso.2023.100604

Welburn SC, Maudlin I. Priorities for the elimination of sleeping sickness. Adv Parasitol. 2012;79:299-337. https://doi.org/10.1016/B978-0-12-398457-9.00004-4

World Health Organization, 2021. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. World Health Organization, Geneva, Switzerland. ISBN: 978 92 4 001035 2. 196p. 

World Health Organization, 2023a. Trypanosomiasis, human African (sleeping sickness): key facts. Accessed at https://www.who.int/news-room/fact-sheets/detail/trypanosomiasis-human-african-(sleeping-sickness) on February 19, 2023.

World Health Organization, 2023b. Human African Trypanosomiasis, (sleeping sickness): the global health observatory. Accessed at https://www.who.int/data/gho/data/themes/topics/human-african-trypanosomiasis on February 19, 2023.

Population genetics of *Glossina palpalis* gambiensis in the sleeping sickness focus of Boffa (Guinea) before and after eight years of vector control: no effect of control despite a significant decrease of human exposure to the diseaseMoise S. Kagbadouno, Modou Séré, Adeline Ségard, Abdoulaye Dansy Camara, Mamadou Camara, Bruno Bucheton, Jean-Mathieu Bart, Fabrice Courtin, Thierry de Meeûs, Sophie Ravel<p style="text-align: justify;">Human African trypanosomosis (HAT), also known as sleeping sickness, is still a major concern in endemic countries. Its cyclical vector are biting insects of the genus Glossina or tsetse flies. In Guinea, the mangro...Disease Ecology/Evolution, Ecology of hosts, infectious agents, or vectors, Evolution of hosts, infectious agents, or vectors, Parasites, Population genetics of hosts, infectious agents, or vectorsHugues Nana Djeunga2023-07-29 13:24:52 View
29 Jan 2024
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Celebrating the 20th Anniversary of the First Xanthomonas Genome Sequences – How Genomics Revolutionized Taxonomy, Provided Insight into the Emergence of Pathogenic Bacteria, Enabled New Fundamental Discoveries and Helped Developing Novel Control Measures – A Perspective from the French Network on Xanthomonads

Advancing Pathogen Genomics: A Comprehensive Review of the Xanthomonas(*) Genome's Impact on Bacterial Research and Control Strategies

Recommended by ORCID_LOGO based on reviews by Boris Vinatzer and 3 anonymous reviewers

The paper titled "Celebrating the 20th Anniversary of the First Xanthomonas Genome Sequences – How Genomics Revolutionized Taxonomy Provided Insight into the Emergence of Pathogenic Bacteria Enabled New Fundamental Discoveries and Helped Developing Novel Control Measures – A Perspective from the French Network on Xanthomonads" by Ralf Koebnik et al. (2023) is an insightful contribution to the field of genomics and its application in understanding pathogenic bacteria, particularly Xanthomonas. This comprehensive review offers a unique perspective from the French Network on Xanthomonads, underscoring the significant advancements in taxonomy, pathogen emergence, and development of control strategies due to genomic research.

One of the paper's main strengths is its thorough exploration of how genomics has revolutionized our understanding of Xanthomonas and other pathogenic bacteria. It sheds light on the evolution and emergence of these pathogens, contributing significantly to the development of novel and effective control measures. The authors' detailed account of the historical progress and current state of genomics in this field highlights its pivotal role in guiding future research and practical applications in managing bacterial diseases.

Moreover, the paper emphasizes the importance of collaborative efforts and the sharing of knowledge within scientific networks, as exemplified by the French Network on Xanthomonas. This approach not only enriches the study but also serves as a model for future collaborative research endeavors.

In conclusion, the work of Koebnik et al. is a valuable resource for researchers, policymakers, and practitioners in the field of plant pathology and genomics. It not only provides a comprehensive overview of the advances in genomics related to Xanthomonas but also illustrates the broader impact of genomic studies in understanding and managing pathogenic bacteria.

References

Ralf Koebnik, Sophie Cesbron, Nicolas W. G. Chen, Marion Fischer-Le Saux, Mathilde Hutin, Marie-Agnès Jacques, Laurent D. Noël, Alvaro Perez-Quintero, Perrine Portier, Olivier Pruvost, Adrien Rieux, And Boris Szurek (2024) Celebrating the 20th anniversary of the first Xanthomonas genome gequences – How genomics revolutionized taxonomy, provided insight into the emergence of pathogenic bacteria, enabled new fundamental discoveries and helped developing novel control measures – A perspective from the French network on Xanthomonads. Zenodo ver. 3, peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.8223857

Celebrating the 20th Anniversary of the First Xanthomonas Genome Sequences – How Genomics Revolutionized Taxonomy, Provided Insight into the Emergence of Pathogenic Bacteria, Enabled New Fundamental Discoveries and Helped Developing Novel Control ...Ralf Koebnik, Sophie Cesbron, Nicolas W. G. Chen, Marion Fischer-Le Saux, Mathilde Hutin, Marie-Agnès Jacques, Laurent D. Noël, Alvaro Perez-Quintero, Perrine Portier, Olivier Pruvost, Adrien Rieux, And Boris Szurek<p>In this Opinion paper, members of the French Network on Xanthomonads give their personal view on what they consider to be some of the groundbreaking discoveries in the field of molecular plant pathology over the past 20 years. By celebrating th...Epidemiology, Evolution of hosts, infectious agents, or vectors, Genomics, functional genomics of hosts, infectious agents, or vectors, Interactions between hosts and infectious agents/vectors, Molecular biology of infections, Molecular genetics o...Damien François Meyer2023-08-09 10:37:15 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
14 Feb 2024
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A Bayesian analysis of birth pulse effects on the probability of detecting Ebola virus in fruit bats

Epidemiological modeling to optimize the detection of zoonotic viruses in wild (reservoir) species

Recommended by ORCID_LOGO based on reviews by Hetsron Legrace NYANDJO BAMEN and 1 anonymous reviewer

Various species of Ebolavirus have caused, and are still causing, zoonotic outbreaks and public health crises in Africa. Bats have long been hypothesized to be important reservoir populations for a series of viruses such as Hendra or Marburg viruses, the severe acute respiratory syndrome coronavirus (SARS-CoV, SARS-CoV-2) as well as Ebolaviruses [2, 3]. However the ecology of disease dynamics, disease transmission, and coevolution with their natural hosts of these viruses is still poorly understood, despite their importance for predicting novel outbreaks in human or livestock populations. The evidence that bats function as sylvatic reservoirs for Ebola viruses is yet only partial. Indeed, only few serological studies demonstrated the presence of Ebolavirus antibodies in young bats [4], albeit without providing positive controls of viral detection or identifying the viral species (via PCR). There is thus an unexplained discrepancy between serological data and viral detection [2, 4]. 

In this article, Pleydell et al. [1] use a modeling approach as well as published serological and age-structure (of the bat population) data to calibrate the model simulations. The study starts with the development of an age-structured epidemiological model which includes seasonal birth pulses and waning immunity, both generating pulses of Ebolavirus transmission within a colony of African straw-coloured fruit bats (Eidolon helvum). The epidemiological dynamics of such system of ordinary differential equations can generate annual outbreaks, skipped years or multi-annual cycles up to chaotic dynamics. Therefore, the calibration of the parameters, and the definition of biologically relevant priors, are key. To this aim, the serological data are obtained from a previous study in Cameroon [5], and the age structured of the bat population (birth and mortality) from a population study in Ghana [6]. These data are integrated into the Bayesian analysis and statistical framework to fit the model and generate predictions. In a nutshell, the authors show an overlap between the data and credibility intervals generated by the calibrated model, which thus explains well the seasonality of age-structure, namely changes in pup presence, number of lactating females, or proportion of juveniles in May. The authors can estimate that 76% of adults and 39% of young bats do survive each year, and infections are expected to last one and a half weeks. The epidemiological model predicts that annual birth pulses likely generate annual disease outbreaks, so that weeks 30 to 31 of each year, are predicted to be the best period to isolate the circulating Ebolavirus in this bat population. From the model predictions, the authors estimate the probability to have missed an infectious bat among all the samples tested by PCR being approximately of one per two thousands. The disease dynamics pattern observed in the serology data, and replicated by the model, is likely driven by seasonal pulses of young susceptible bats entering the population. This seasonal birth event increases the viral transmission, resulting in the observed peak of viral prevalence. With the inclusion of immunity waning and antibody persistence, the model results illuminate therefore why previous studies have detected only few positive cases by PCR tests, in contrast to the evidence from serological data. 

 This study provides a first proof of principle that epidemiological modeling, despite its many simplifying assumptions, can be applied to wild species reservoirs of zoonotic diseases in order to optimize the design of field studies to detect viruses. Furthermore, such models can contribute to assess the probability and timing of zoonotic outbreaks in human or livestock populations. This article illustrates one of the manifold applications of mathematical theory of disease epidemiology to optimize sampling of pathogens/parasites or vaccine development and release [7, 8]. The further coupling of such models with population genetics theory and statistical inference methods (using parasite genome data) increasingly provide insights into the adaptation and evolution of parasites to human, crops and livestock populations [9, 10].

 

References

[1] Pleydell D.R.J., Ndong Bass I., Mba Djondzo F.A., Djomsi D.M., Kouanfack C., Peeters M., and J. Cappelle. 2023. A Bayesian analysis of birth pulse effects on the probability of detecting Ebola virus in fruit bats. bioRxiv, ver. 3 peer reviewed and recommended by Peer Community In Infections. https://doi.org/10.1101/2023.08.10.552777

[2] Caron A., Bourgarel M., Cappelle J., Liégeois F., De Nys H.M., and F. Roger. 2018. Ebola virus maintenance: if not (only) bats, what else? Viruses 10, 549. https://doi.org/10.3390/v10100549

[3] Letko M., Seifert S.N., Olival K.J., Plowright R.K., and V.J. Munster. 2020. Bat-borne virus diversity, spillover and emergence. Nature Reviews Microbiology 18, 461–471. https://doi.org/10.1038/s41579-020-0394-z

[4] Leroy E.M., Kumulungui B., Pourrut X., Rouquet P., Hassanin A., Yaba P., Délicat A., Paweska J.T., Gonzalez J.P., and R. Swanepoel. 2005. Fruit bats as reservoirs of Ebola virus. Nature 438, 575–576. https://doi.org/10.1038/438575a

[5] Djomsi D.M. et al. 2022. Dynamics of antibodies to Ebolaviruses in an Eidolon helvum bat colony in Cameroon. Viruses 14, 560. https://doi.org/10.3390/v14030560

[6] Peel A.J. et al. 2016. Bat trait, genetic and pathogen data from large-scale investigations of African fruit bats Eidolon helvum. Scientific data 3, 1–11. https://doi.org/10.1038/sdata.2016.49

[7] Nyandjo Bamen H.L., Ntaganda J.M., Tellier A. and O. Menoukeu Pamen. 2023. Impact of imperfect vaccine, vaccine trade-off and population turnover on infectious disease dynamics. Mathematics, 11(5), p.1240. https://doi.org/10.3390/math11051240

[8] Saadi N., Chi Y.L., Ghosh S., Eggo R.M., McCarthy C.V., Quaife M., Dawa J., Jit M. and A. Vassall. 2021. Models of COVID-19 vaccine prioritisation: a systematic literature search and narrative review. BMC medicine, 19, pp.1-11. https://doi.org/10.1186/s12916-021-02190-3

[9] Maerkle, H., John S., Metzger, L., STOP-HCV Consortium, Ansari, M.A., Pedergnana, V. and Tellier, A., 2023. Inference of host-pathogen interaction matrices from genome-wide polymorphism data. bioRxiv, https://doi.org/10.1101/2023.07.06.547816.

[10] Gandon S., Day T., Metcalf C.J.E. and B.T. Grenfell. 2016. Forecasting epidemiological and evolutionary dynamics of infectious diseases. Trends in ecology & evolution, 31(10), pp.776-788. https://doi.org/10.1016/j.tree.2016.07.010

A Bayesian analysis of birth pulse effects on the probability of detecting Ebola virus in fruit batsDavid R.J. Pleydell, Innocent Ndong Bass, Flaubert Auguste Mba Djondzo, Dowbiss Meta Djomsi, Charles Kouanfack, Martine Peeters, Julien Cappelle <p>Since 1976 various species of Ebolavirus have caused a series of zoonotic outbreaks and public health crises in Africa. Bats have long been hypothesised to function as important hosts for ebolavirus maintenance, however the transmission ecology...Animal diseases, Disease Ecology/Evolution, Ecohealth, Ecology of hosts, infectious agents, or vectors, Epidemiology, Population dynamics of hosts, infectious agents, or vectors, Reservoirs, Viruses, ZoonosesAurelien Tellier2023-08-16 16:57:05 View