# Reflection on the ultimate effects of rabies elimination in western Europe in the context of ‘One Health’ and ‘Nexus’

Patrick Giraudoux

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## To cite this version:

Patrick Giraudoux. Reflection on the ultimate effects of rabies elimination in western Europe in the context of ‘One Health’ and ‘Nexus’. Bulletin de l’Académie Vétérinaire de France, 2025, epub, pp.7-11. 10.3406/bavf.2025.71149. hal-05277826

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# REFLECTION ON THE ULTIMATE EFFECTS OF RABIES ELIMINATION IN WESTERN EUROPE IN THE CONTEXT OF 'ONE HEALTH' AND 'NEXUS' *

## RÉFLEXION SUR LES EFFETS ULTIMES DE L'ÉLIMINATION DE LA RAGE EN EUROPE OCCIDENTALE DANS LE CONTEXTE « ONE HEALTH » ET « NEXUS »

Patrick GIRAUDOUX*

The initial manuscript was received on August 7th 2025, and the revised version was received on August 12th 2025, and accepted on August 13th 2025; the editorial revision was on August 15th 2025.

## ABSTRACT

This article analyzes the unexpected effects of the elimination of fox rabies in Europe from a "One Health" and "Nexus" perspective. The elimination of rabies along with other concomitant factors led to a surge in fox populations in the 1980s, promoting the transmission of other animal diseases, such as sarcoptic mange, distemper and a parasitic zoonosis, alveolar echinococcosis, the colonization of cities by this species, and possibly greater exposure of certain prey species to predation. This dynamic illustrates the unexpected cascading effects of a health policy targeting a single element of a socio-ecosystem and thus shows that decisions focused on a single aspect of health can have repercussions on other aspects of the socio-ecosystem. This article therefore advocates for integrated, interdisciplinary and adaptive governance capable of managing the complex interdependencies between human, animal and ecosystem health at various scales.

**Keywords:** rabies, fox, echinococcosis, One Health, socio-ecosystem

## RÉSUMÉ

Cet article analyse les effets inattendus de l'élimination de la rage vulpine en Europe dans une perspective « One Health » et « Nexus ». L'élimination de la rage, associée à d'autres facteurs concomitants, a entraîné un accroissement démographique des populations de renards dans les années 1980, favorisant la transmission d'autres maladies animales telles que la gale sarcoptique et la maladie de Carré et une zoonose parasitaire, l'échinococcose alvéolaire, la colonisation des villes par cette espèce, et possiblement une exposition plus grande de certaines espèces-proies à la prédation. Cette dynamique illustre les effets en cascade inattendus d'une politique sanitaire ciblée sur un seul élément d'un socio-écosystème, et montre ainsi que des décisions focalisées sur un seul aspect de la santé peuvent avoir des répercussions sur d'autres aspects du socio-écosystème. Cet article plaide ainsi pour une gouvernance intégrée, interdisciplinaire et adaptative, capable de gérer les interdépendances complexes entre la santé humaine, animale et écosystémique à différentes échelles.

**Mots-clés :** rage, renard, échinococcose, Une seule santé, socio-écosystème

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<footnote>* This article was written, extensively supplemented and enriched, based on the supplementary material from the following article: Giraudoux et al. (2025b) published in Open Forum Infectious Diseases (https://doi.org/10.1093/ofid/ofaf310).</footnote>

<footnote>1- Professeur émérite d'écologie, UMR UFC/CNRS Chrono-environnement, Université Marie et Louis Pasteur, Besançon, France.</footnote>

<footnote>Courriel : patrick.giraudoux@univ-fcomte.fr</footnote>
# INTRODUCTION

The One Health framework, jointly approved in 2023 by the World Health Organisation, the World Organisation for Animal Health, the Food and Agriculture Organisation of the United Nations, and the United Nations Environment Programme, is defined as an “integrated and unifying approach that aims to sustainably balance and optimize the health of people, animals and ecosystems.” Although the ultimate question is that of the planet's habitability for humans, this definition introduces a change in perspective: human health is no longer the sole priority, but must be balanced and optimized jointly with the health of animals, plants and ecosystems. This raises certain practical and ethical questions (Giraudoux et al. 2025a, 2025b). Furthermore, in December 2024, the 147 member states of IPBES (Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services)—now numbering 150—approved the summary for policymakers of the Nexus report, which examines the links between biodiversity, water, food and health in the context of climate change (IPBES et al. 2025a). This report, which provides more than 70 options for breaking away from silo approaches, highlights that these approaches cost between 10 and 20% of global GDP. Thus, in view of the challenges of this century, the Nexus approach brings together five elements and their relationships, which are usually dissociated in conventional thinking, into a single world. It integrates, in a pragmatic and rigorous manner, the factorial complexity of nested time and space scales, and thus reconciles the framework of current interdisciplinary approaches, such as One Health, Planetary Health, Global Health, and EcoHealth (health ecology) (IPBES et al. 2025a).

Recent events corroborate these approaches and show that it is problematic to legislate in one area without considering the effects of legislation on other areas. Agriculture, for example, must be thought of in terms of a “food system” in its interdependencies with biodiversity, water, and human, animal and plant health, in the context of global warming. However, this injunction and the urgent need to break down barriers in decision-making still come up against a form of disbelief, even political denial of these dependencies, as well as the comfort of habit. Finally, they come up against the difficulty of predicting with certainty a particular local effect in a complex system (how far can we go in terms of complexity?), where many trajectories of change are possible, and where the measured concomitances and correlations are not necessarily direct causal relationships, which are difficult to isolate due to this very high complexity, the multifactorial nature of the processes involved and the circularity of certain causes.

However, it is possible to learn from a retrospective analysis of case studies involving long-term longitudinal monitoring (see, for example, Giraudoux et al. (2024), in this Bulletin, on alveolar echinococcosis in southern Gansu, China).

The aim of this article is to briefly present such a case study, examining the evolution of fox populations in continental Europe over the last 60 years, and how this evolution may have changed the way questions and answers relating to human, animal and socio-ecosystem health are approached.

# FOX RABIES IN CONTINENTAL EUROPE

In the second half of the 20th century, red fox (Vulpes vulpes) populations experienced a rabies epidemic throughout continental Europe. The first cases of rabies in wildlife (foxes and wolves) were observed in 1951 in three districts of eastern Latvia (Wandeler 2004), and the disease spread south-west toward Poland, with the front of the epizootic then moving about 20–60 km per year. The first cases were reported in Germany in 1947, Belgium and Luxembourg in 1966, Switzerland in 1967, France in 1968, and the Netherlands in 1974 (Delcourt et al. 2022). Hunting before the outbreak (fox pelts were valuable at the time), the outbreak itself and its management kept fox populations relatively low throughout Europe until the early 1980s. Although no fatal autochthonous human cases were reported during more than 30 years epidemic due to the lower infectivity of the virus strain to non-fox species, efficient prevention campaigns, and human post-exposure treatment, a response in all these countries was to try to reduce the fox population further (shooting, trapping, poisoning, and gassing), but this failed to stop the epizootic and actually accelerated its spread on the western front. To reduce public health risks to humans and domestic animals, oral fox rabies vaccines were developed. From the mid-1980s, large-scale fox vaccination campaigns were conducted to successfully eliminate fox rabies in Western Europe. The last case of fox rabies was recorded in 1998 in France, 2001 in Germany, and, in 2018, fox rabies was officially considered eliminated from most of the EU territory. The front is now on the eastern border of the EU, from Estonia to Romania.

# IMMEDIATE CONSEQUENCES OF RABIES CONTROL ON FOX POPULATIONS

The vaccination campaigns were followed by a demographic surge, and the fox populations became much larger than before the outbreak. Rabies vaccination alone was not the direct cause of this demographic explosion, as it also occurred decades earlier in rabies-free areas, like in the UK. The causes are more likely to be a combination of human-induced environmental changes that could benefit the continental fox population, once rabies has been eliminated and the subsequent systematic and massive culling of foxes has ended (Delcourt et al. 2022). This demographic explosion was followed by the emergence of urban fox populations throughout Europe. Rural fox populations now seem to have reached densities close to carrying capacity, and populations have stabilized, but they fluctuate locally due to local epizootics of sarcoptic mange and distemper.

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# FOXES ON THE RISE: WHEN PUBLIC HEALTH RESHAPES THE SOCIO-ECOSYSTEM

The red fox is one of the most widespread generalist mesopredators in Western Europe. Eurasia is part of its natural range, where the species has co-evolved for hundreds of thousands of years with other species in the ecosystems to which it belongs (Statham *et al.* 2014). However, foxes can exert significant predation pressure on their prey. They feed on small mammals, that's why they are considered beneficial by some farmers (for example in regions where voles are crop pests; Giraudoux & Couval 2024), and on many birds, particularly ground-nesting species (Lindström *et al.* 1994; Tryjanowski *et al.* 2002), which leads poultry farmers to consider them as a nuisance (Pépin *et al.* 2025). Locally, they can be one of the main causes of mortality among roe deer (*Capreolus capreolus*) fawns (Lindström *et al.* 1994; Jarnemo *et al.* 2004) and lambs (White *et al.* 2000). This makes it a major target in predator control, particularly in regions where hunting programs are implemented, for example in the hope of developing small game (European hare *Lepus europeus*, Phasianidae, etc.) (Panek *et al.* 2006) or to protect waterbirds, such as the Eurasian curlew (*Numenius arquata*) and the northern lapwing (*Vanellus vanellus*), or mammals such as the European hamster (*Cricetus cricetus*) in Alsace.

Moreover, the continental increase in the fox population coincided with the geographical expansion of the parasite *Echinococcus multilocularis* in Western Europe (Combes *et al.* 2012), its urbanization (Liccioli *et al.* 2015), and an increase in the incidence of human alveolar echinococcosis (Schweiger *et al.* 2007; Deplazes *et al.* 2017; Knapp *et al.* 2025). Evidence has been provided that regulating the circulation of the parasite by the usual means of shooting or trapping foxes is ineffective and even counterproductive (Comte *et al.* 2017). Other studies suggest that achieving the desired reduction in parasite circulation through sustained suppression of the fox population to very low levels would require measures that are ethically, logistically, and ecologically unacceptable (Raoul *et al.* 2003; Jiguet 2020; Giraudoux *et al.* 2020b; ANSES 2023). Actually, an optimal form of prevention comprises encouraging people not to handle foxes, fence off gardens, and deworm dogs and cats. Additional prophylactic measures can even be applied locally if necessary, such as deworming by baiting foxes that frequent the surroundings of homes (Comte *et al.* 2013; Craig *et al.* 2017), with the advantage of not destabilizing their population and, therefore, not leaving the space empty for new infested arrivals, but it raises the question of the long-term ecological effects of systematic deworming, which have not been studied.

Another troubling issue concerns the role attributed to foxes in regulating grassland vole outbreaks and Lyme disease. Indeed, stakeholders who wish to see less persecution of the species (it is still classified as a "species likely to cause damage" [ESOD] in many departments in France) often argue that it is a predator of voles, which is undeniable, and that it is 'likely to limit outbreaks that are undesirable for farmers'. They also cite two studies to attribute to it an additional role as an indirect regulator of pathogens such as *Borrelia* sp., which causes Lyme disease (Levi *et al.* 2012; Hofmeester *et al.* 2017). However, this latter point is contradicted by another study that presents it as a reservoir for *Borrelia* sp. (Lesiczka *et al.* 2023). Knowledge is therefore still far from stable, and all the ecological idiosyncrasies and complexities are far from being identified and understood. In reality, however, it is striking to note that this long post-rabies period of increasing fox populations has not led to a decrease in the amplitude and frequency of mountain water vole (*Arvicola amphibius*) outbreaks in the Jura Mountains, where fox densities reach some of the highest values observed in rural areas in Europe (Berthier *et al.* 2014; Giraudoux *et al.* 2020b; Giraudoux & Couval 2024), nor to a decrease in the incidence of Lyme disease, which has actually almost doubled in France since the beginning of the XXIst century (Nuttens *et al.* 2023).

These findings therefore call into question any simplistic interpretation of the isolated effect of a particular species, such as the fox, on a socio-ecosystem, given that these regulatory processes are most often community-based, multifactorial processes involving dozens of species (Hansson & Henttonen 1988; Giraudoux *et al.* 2020b et https://zaaj.univ-fcomte.fr/spip.php?article118; Boulanger 2021). In addition, changes in the socio-ecosystem involve many concomitant variables: changes in agricultural practices, including increased grassland productivity with regard to rodent population outbreaks in the Jura (Giraudoux 2022), explosive growth in populations of all types of ungulates (roe deer, wild boar, red deer, chamois, etc.), potential hosts of adult ticks, which occurred during the same period due to the mandatory implementation of hunting plans since 1978.

Nevertheless, the characteristics of today's post-rabies socio-ecosystems, in which fox populations play a role, are very different from those of the pre-rabies period, when these populations existed at relatively low densities (Giraudoux 2025).

# CONCLUSION: CONSIDERING CASCADING EFFECTS AND THE GOVERNANCE OF INTERDEPENDENCIES

In the context of One Health, the example presented here shows how what is good for one target can be harmful to others. Here, the fight against a potential threat to human health, in this case rabies in foxes, along with other concomitant factors, triggered a cascade of consequences for epizootics, such as sarcoptic mange and canine distemper, as well as the strengthening of a parasitic zoonosis, alveolar echinococcosis. In addition, the change in fox population dynamics, again in conjunction with other factors, may have had an impact on certain endangered species and small game (Giraudoux *et al.* 2020b; Delcourt *et al.* 2022). However, it has not had the expected effects, where these have been measured over the long term, on multi-year variations in vole populations and on the incidence of Lyme disease.

AVF

Bull. Acad. Vét. France — 2025

http://www.academie-veterinaire-defrance.org/
Like those presented in Giraudoux et al. (2025a, 2025b), this case study illustrates “the essential link between human, domestic animal and wildlife health”. Like them, it also highlights why managing such complex systems requires “mobilizing multiple sectors, disciplines and communities at different levels of society to work together” (OHHLEP et al. 2022), in order to anticipate and prevent the undesirable consequences of decisions taken concerning a single element of the “One Health” triptych while neglecting the others. “Balancing and sustainably optimizing the health of people, animals and ecosystems” (OHHLEP et al. 2022) is not only a matter for doctors and veterinarians, but for a much broader section of society, with inevitable trade-offs between different health and non-health outcomes to be considered at multiple scales of time and space. The concept of a multi-partner working group is essential to implement here (Brown et al. 2024; Giraudoux et al. 2020a).

These findings should also encourage us to consider human, animal and ecosystem health globally, not only in terms of inter-dependencies, but also in terms of hierarchical organization within a cascade of constraints and feedback mechanisms. This raises the question of what form of governance can ensure effective coordination between all stakeholders and how non-human entities can be represented in such a deliberative framework (Giraudoux et al. 2025a, 2025b). To our knowledge, the means of resolving the prominent normative and ethical dilemma of the OHHLEP’s “One Health” definition remain to be established. Recent IPBES assessments on the Nexus and transformative changes (IPBES et al. 2025a, 2025b) have emphasized that the best way to overcome single-issue silos is to use integrated and adaptive decision-making, known as the “Nexus approach.” The One Health concept is undoubtedly a special case of the Nexus approach, but relevant governance organizations capable of addressing these issues in a cross-cutting manner have yet to be invented.

ACKNOWLEDGEMENTS

*The author thanks Denis Malvy for his constructive review of the manuscript.*

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