Zoonotic pathogens, those transmitted from animals to humans, constitute a major public health risk with high associated global economic costs. Diseases associated with these pathogens represent more than 60% of emerging infectious diseases and predominantly originate in wildlife (1). Over the last decades, the emergence and re-emergence of zoonotic pathogens have led to an increasing number of epidemics, as illustrated by the current Covid-19 pandemic. There is ample evidence that human impact on native ecosystems such as deforestation, agricultural development, and urbanization, is linked to spillover of pathogens from animals to humans (2). However, research and calls to action have mainly focused on the importance of surveillance and prevention of zoonotic emergences along landscape interfaces, with special emphasis on tropical forests and agroecosystems, and studies and reviews pointing out the zoonotic risk associated with cities are scarce.  Additionally, cities are sometimes wrongly seen as one homogeneous ecosystem, almost exclusively human, with a Northern hemisphere-biased perception of what a city is, which fails to take into account the ecological and socio-economic diversities that can constitute an urban area.

Here, Dobigny and Morand (3) aim to draw attention to the importance of urban ecosystems in zoonotic risk and advocate that further attention should be paid to urban, peri-urban and suburban areas. In this well-organized and well-documented review, the authors show, using updated literature, that cities are places where massive contacts occur between wildlife, domestic animals, and human inhabitants (thus constituting spillover opportunities), and that it is even likely that human and wildlife contact in urban centers is more prevalent than in wild areas, perhaps contrary to intuition. Indeed, cities currently constitute the most important environment of human life and are places for millions of close interactions between humans and animals, including pets and domestic animals, wild animals through the intrusion of wild urban-adapted species (e.g., some bat, rodent, or bird species among others), manipulation and consumption of wildlife meat, and the existence of wildlife meat markets, which all constitute a major risk for zoonotic spillover. In cities, lab escapees of zoonotic pathogens also exist, and trends of adaptation to urban ecological conditions of many vectors of primary health importance is also a concern. The authors further argue that cities are predominant places for both epidemic amplification of human-human transmitted pathogens, because they are places with high human densities and population growth, and for dissemination of reservoirs, vectors and pathogens, as they are transport hubs. Dobigny & Morand further predict, likely correctly, that cities may be important places for pathogen evolution.  Finally, they propose actions and recommendations to limit the risk of zoonotic spillover events from urban ecosystems and future directions for research aiming at assessing this risk. 

The reviewers found the manuscript well-organized and presented, timely, and bringing novel contributions to the field of zoonotic emergence. I strongly recommend this article, which should benefit a large audience, particularly in the context of the current Covid-19 pandemics and the ongoing One Health initiatives aiming at preventing future zoonotic disease emergence (4). 

References

(1) Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature, 451, 990–993. https://doi.org/10.1038/nature06536

(2) White RJ, Razgour O (2020) Emerging zoonotic diseases originating in mammals: a systematic review of effects of anthropogenic land-use change. Mammal Review, 50, 336–352. https://doi.org/10.1111/mam.12201

(3) Dobigny G, Morand S (2022) Zoonotic emergence at the animal-environment-human interface: the forgotten urban socio-ecosystems. Zenodo, 6444776, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.5281/zenodo.6444776

(4) Morand S, Lajaunie C (2021) Biodiversity and COVID-19: A report and a long road ahead to avoid another pandemic. One Earth, 4, 920–923. https://doi.org/10.1016/j.oneear.2021.06.007

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.

Deciphering the virome (the set or assemblage of viruses) of the Earth, from individual organisms to entire ecosystems, has become a key priority. The first step to better understanding the impact of viruses on the ecology and functions of ecosystems is to describe their diversity. Such knowledge opens the gates to a better assessment of global nutrient cycling or of the threat that viruses represent to individual health. This explains the increasing number of pioneering studies that are currently sequencing the complete or partial genome of thousands of new viruses [1].

In their exciting study, Fritz and collaborators [2], authors sampled 209 army ants (Genus Dorylus) to investigate the virus diversity in dense forests that researchers cannot easily access. Indeed, these ants live in colonies (21 were sampled) that can move 1 km per day, covering a significant area and attacking many invertebrate and vertebrate preys.  Each sample was sequenced by a protocol called VANA sequencing and allowing the enrichment of the sample in viral sequences [3], so improving the detection of viruses present at low abundance in the ant (and more specifically in its gut for viruses infecting preys). 

Around 45,000 contigs presented homologies with bacterial, plant, invertebrate, and vertebrate infecting viruses. Half could be assigned to 56 families and 157 genera of the International Committee on Taxonomy of Viruses. Beyond this amazing harvest of new and known virus sequences using an original methodology, the results significantly improve the current frontiers of known viral taxonomy and diversity and raise exciting research tracks to expand them. 

As a preprint, several blogs or news of leading scientists and journals have already highlighted this study. For example, in the news section of Science magazine, Jon Cohen underlined the originality of the approach for virus hunting on Earth with the title “Armed with air samplers, rope tricks, and—yes—ants, virus hunters spot threats in new ways”[4]. Another example is the mention of the publication by Elisabeth Bik in her Microbiome Digest: she wrote, “An amazing read is a fresh preprint from Fritz and collaborator describing an exciting method of sampling in difficult-to-reach environments“ [5].

The paper from Fritz et al [2] thus represents a significant advance in virus ecology, as already recognized by early readers, and this is why I strongly recommend its publication in PCI Infections.

REFERENCES

1. Edgar RC, Taylor J, Lin V, Altman T, Barbera P, Meleshko D, Lohr D, Novakovsky G, Buchfink B, Al-Shayeb B, Banfield JF, de la Peña M, Korobeynikov A, Chikhi R, Babaian A (2022) Petabase-scale sequence alignment catalyses viral discovery. Nature, 602, 142–147. https://doi.org/10.1038/s41586-021-04332-2

2. Fritz M, Reggiardo B, Filloux D, Claude L, Fernandez E, Mahé F, Kraberger S, Custer JM, Becquart P, Mebaley TN, Kombila LB, Lenguiya LH, Boundenga L, Mombo IM, Maganga GD, Niama FR, Koumba J-S, Ogliastro M, Yvon M, Martin DP, Blanc S, Varsani A, Leroy E, Roumagnac P (2023) African army ants at the forefront of virome surveillance in a remote tropical forest. bioRxiv, 2022.12.13.520061, ver. 4 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.12.13.520061

3. François S, Filloux D, Fernandez E, Ogliastro M, Roumagnac P (2018) Viral Metagenomics Approaches for High-Resolution Screening of Multiplexed Arthropod and Plant Viral Communities. In: Viral Metagenomics: Methods and Protocols Methods in Molecular Biology. (eds Pantaleo V, Chiumenti M), pp. 77–95. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-7683-6_7

4. Cohen J (2023) Virus hunters test new surveillance tools. Science, 379, 16–17. https://doi.org/10.1126/science.adg5292

5. Ponsero A (2023) February 18th, 2023. Microbiome Digest - Bik’s Picks. https://microbiomedigest.com/2023/02/18/february-18th-2023/

​​Diptera-borne pathogens rank among the most serious health threats to vertebrate organisms around the world, particularly in tropical areas undergoing strong human impacts – e.g., urbanization and farming –, where social unrest and poor economies exacerbate the risk (Allen et al. 2017; Robles-Fernández et al. 2022). Although scientists have acquired a detailed knowledge on the life-history of malaria parasites (Pacheco and Escalante 2023), they still do not have enough information about their insect vectors to make informed management and preventive decisions (Santiago-Alarcon 2022).

In this sense, I am pleased to recommend the study of Vantaux et al. (2023), where authors conducted an experimental and theoretical study to analyzed how the diversity of blood sources (i.e., human, cattle, sheep, and chicken) affected the fitness of the human malaria parasite – Plasmodium falciparum – and its mosquito vector – Anopheles gambiae s.l.

The study was conducted in Burkina Faso, West Africa. Interestingly, authors did not find a significant effect of blood meal source on parasite development, and a seemingly low impact on the fitness of mosquitoes that were exposed to parasites. However, mosquitoes’ feeding rate, survival, fecundity, and offspring size were negatively affected by the type of blood meal ingested. In general, chicken blood represented the worst meal source for the different measures of mosquito fitness, and sheep blood seems to be the least harmful. This result was supported by the theoretical model, where vectorial capacity was always better when mosquitoes fed on sheep blood compared to cow and chicken blood. Thus, the knowledge generated by this study provides a pathway to reduce human infection risk by managing the diversity of farm animals. For instance, transmission to humans can decrease when chickens and cows represent most of the available blood sources in a village.

These results along with other interesting details of this study, represent a clear example of the knowledge and understanding of insect vectors that we need to produce in the future, particularly to manage and prevent hazards and risks (sensu Hoseini et al. 2017).

REFERENCES

Allen T., et al., Global hotspots and correlates of emerging zoonotic diseases. Nat. Commun. 8, 1124. (2017). https://doi.org/10.1038/s41467-017-00923-8

Hosseini P.R., et al., Does the impact of biodiversity differ between emerging and endemic pathogens? The need to separate the concepts of hazard and risk. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160129 (2017). https://doi.org/10.1098/rstb.2016.0129

Pacheco M.A., and Escalante, A.A., Origin and diversity of malaria parasites and other Haemosporida. Trend. Parasitol. (2023) https://doi.org/10.1016/j.pt.2023.04.004

Robles-Fernández A., et al., Wildlife susceptibility to infectious diseases at global scales. PNAS 119: e2122851119. (2022). https://doi.org/10.1073/pnas.2122851119

Santiago-Alarcon D. A meta-analytic approach to investigate mosquitoes’ (Diptera: Culicidae) blood feeding preferences from non-urban to urban environments. In: Ecology and Control of Vector-borne Diseases, vol. 7 (R.G. Gutiérrez-López, J.G. Logan, Martínez-de la Puente J., Eds). Pp. 161-177. Wageningen Academic Publishers. eISBN: 978-90-8686-931-2 | ISBN: 978-90-8686-379-2 (2022).

Vantaux A. et al. Multiple hosts, multiple impacts: the role of vertebrate host diversity in shaping mosquito life history and pathogen transmission. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Infections (2023). https://doi.org/10.1101/2023.02.10.527988

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