One Health or ‘One Health washing’? An alternative to overcome now more than ever

Researchers apparently studying ecological interaction often remain focused on technical and biological enquiries with no obvious link to other disciplines. For example, virus hunters, though technologically armed, often lack appropriate ecological elements and thus sufficient knowledge of the socio-ecosystems they explore for virus outbreaks (actual or potential), thus rapidly becoming overwhelmed by the huge diversity of existing viruses and by the magnitude of the task. An illustration of this can be given here: to understand viral phylogeny, an inventory conducted from 2006 to 2018 in 18 provinces of Thailand, Laos and Cambodia, using high-throughput sequencing (HTS), identified in the lungs of 3284 rodent and insectivore specimens 495,579 sequences belonging to 98 distinct RNA virus families (Wu et al., 2021). In the Haut-Doubs, France, 3284 rodents can be easily found in less than 4 hectares during the peak of a population outbreak of a single species, the mountain water vole, Arvicola amphibius. At this specific location, Villette et al. (2020) identified, also using HTS, 155 potentially pathogenic bacterial taxa representing at least 13 genera belonging to 11 families in the 869 specimens sampled, further showing that individual microbial taxon richness depends on the number and type of organs sampled (Villette et al., 2017). Villette (2018) also showed how bacterial communities changed both over a cycle of a few years, and over a time step of about 15 years from one cycle to another.

With the increase in knowledge of new Coronavirus taxa in recent years, we realize that we do not know the existence of the viral isolates of 75% of them, because the work is based solely on the description of global genome sequences and not the discovery of viral particles. By contrast, basic knowledge of infectiology, e.g. on the importance of the size of the viral or bacterial inoculum, is literally disappearing (Guégan, 2022a). It is also known that those microbes are no exception and therefore have extremely rapid evolutionary capabilities, as shown, for example, by the succession of SARS-CoV-2 variants within some months (Giraudoux, 2021). For only those reasons, a viral snapshot obtained at a given month in a place can be different some months later and cannot constitute alone a generality.

In the Haut-Doubs, where temperate ecosystems are much simpler than those of the tropics, the monitoring of a predator–prey community for 20 years showed the existence of cycles of abundance in prey (two main species of voles) alternating for several years between periods of extremely low density (0 to a few individuals per hectare) and extremely high density (several hundred of individuals per hectare). These ‘cycles‘ are followed by consecutive variations in the diet and abundance in the predator community. This study shows that the composition of the predator community itself changed drastically between the beginning and the end of the study (Giraudoux et al., 2020).

What can we learn about the emergence of a few thousand, or even hundreds of thousands, let alone millions of microbial genomes at a given time in ecosystems where we know nothing about the host population dynamics in space and time, the variations in the structure of animal communities, and the relationships and anthropological conditions that bring the multiple components of the system into contact and generate the ground on which disease emergence and outbreak may flourish? What we know about the ecology of these systems ensures that their stability is only apparent, and that their functioning is based on the succession of innumerable emergences and invisible extinctions of local populations, whether they are hosts or their microbes.

Without data on the levels of seasonal and inter-annual fluctuations of host populations, and without anthropological analysis of exposures in the de facto incommensurability of pathogen candidates, it is impossible to detect rapidly the ecosystem changes that are both the cause and the consequences of disease agent emergence.

One Health is a concept that has been promoted for more than 20 years under this term (Zinsstag, 2012; Lerner and Berg, 2017). As the links between ecological and climatic alterations, pathogen emergence, and epidemics of all types have become evident (Morand, 2020; Mendenhall, 2020), scientists and governments around the world have recognized that greater interdisciplinary collaboration is needed to prevent and control most notably, but not exclusively, zoonotic diseases. Two thousand four hundred years after the Hippocratic treatise ‘of airs, waters and places’, and after the more recent hygienic approaches of the great Pasteurian era and their extensions in the eco-epidemiological approach promoted in the 1960s–1970s by Jean-Antoine Rioux and others (Rioux et al., 1981; Schwabe, 1981; Houin et al., 2018), it (re)appears that the functioning of socio-ecosystems at all scales is a determining factor in the emergence of epidemics. It is therefore logical to consider animal and human health with ecosystem health in an integrative whole, and to translate this concept into practice in the field. However, it must be recognized that there is still a long way to go to achieve fully functional integration (Destoumieux-Garzón et al., 2018; Morand et al., 2020; Giraudoux, 2022c).

The study of ecosystem health, like that of human and animal health, requires a material and human investment that is far from being made. For example, investment in Ebola and Marburg virus research between 1997 and 2015 is estimated at US$1035 million, of which 61.3% was allocated to research on vaccines, 29.2% to research on new therapeutics and 9.5% to research on diagnostic kits (Fitchett et al., 2016). We were unable to find figures estimating the investment in ecological and anthropological research on socio-ecosystems and animal population dynamics in the areas affected by these viruses, and we are aware of only a few ongoing ecological studies (e.g. the EBO-SURSY programme; https://rr-africa.oie.int/fr/projets/ebo-sursy-fr). The gap between the two types of investment in research is simply abysmal. At most, when health crises infringe on public awareness, we are fishing for viruses and their nucleic acid barcodes in ecosystems in which host community ecology is virtually unknown at the appropriate scales and levels of biological organization (Wu et al., 2021; Giraudoux, 2022c). One can only deplore this and the consequences, which make the One Health tripod currently work, at best, only on the two legs of human and veterinary health and very exceptionally on all three judiciously claimed supports (Giraudoux, 2022a; Guégan, 2022b). Fasina et al. (2021), in comparing the 145 One Health initiatives deployed in 47 African countries, highlight the poor levels of collaboration between the research networks studied, and how little they take into account, in the vast majority, the environmental components and, surprisingly, do not engage the various stakeholders necessary to achieve the intended goals.

We still have the despairing impression that few researchers are committed to the One Health path, and without the necessary institutional support. Basically, we are still under the illusion that a multidisciplinary programme should have the same cost and the same standard duration of 3–5 years as a conventionally managed research programme, and that One Health is a matter of achieving economies of scale. Often, triggered by proposal call in a general context where research funding sources are scarce, collaborations are only circumstantial and opportunistic, and on a short-term basis. The reality of the needs is quite different: the cost of a multidisciplinary programme is multiplied by the number of disciplines, and it must be conducted by people who have the culture and experience of the interfaces of disciplines and of the margins of their comfort zone, over a long period corresponding to that of the underlying demographic and sociological processes (>10–20 years most often). It must have a unit of place so that the dynamics of the components of the socio-ecosystem can be studied synchronously. And several locations must be monitored to make relevant comparisons.

One Health is a relevant concept to address the challenge and move towards better public, animal and ecological health outcomes. It requires extending the current collaborations between medical and veterinary fields to other relevant expertise, e.g. wildlife ecologists, taxonomists, anthropologists, geographers, etc., well identified by the quality of their publications and experience, and concerned with human, animal and ecosystem health. It also needs the release of significant funds in each area for long-term monitoring and research. Otherwise, business as usual, One Health will remain in the middle of the road as an aspiration, will be the pretext for ‘One Health washing’ (a formula analogous to green washing) to justify other types of research, and will not achieve its promising objectives. It will then quickly pass from incantation to oblivion in international public health.

We welcome the rebound in the international perception of the issues, which is currently motivating WHO, WOAH, FAO and UNEP to jointly advocate a rebalancing of the components of One Health, explicitly including the notion of equity between sectors and disciplines, and a clearer ecological vision of the whole. Without sadness or regret, but based on repeated experience, we are still aware of the effort needed at other levels (international and national administrations, institutions, etc.) to break down the research and administration structural silos, the bureaucratic layers, and internal corporatisms, which still complicate, or even prevent, the implementation of this type of research. A major effort is also needed to finally release the resources (humans, budgets) commensurate with the objectives. The challenges are therefore certainly less conceptual than organizational and structural. The scientific fronts have been identified: the articulation of disciplines for the study of complex socio-ecosystems, the questions raised by changes in temporal and spatial scales, considering the long term. They also emerge directly and counter to the examples given above, as clearly shown in Figure 1. In our opinion, the organizational elements and budgetary trade-offs are also among the prospective elements to be considered most seriously to give substance to this momentum that WHO-WOAH-FAO-UNEP rightly wish to increase.