Introduction

Controlling animal health (Box 1) is essential in animal production and addresses a threefold challenge: optimising the production cycle and reducing losses (economic challenge), contributing to the well-being of animals by taking care of them (ethical challenge) and limiting the emergence of zoonoses (public health challenge). Since their discovery in the 1930s, antibiotics and antiparasitic agents, which respectively control infectious diseases of bacterial origin and parasites, have been essential elements of animal health management. In animal production, they are used to treat an infected animal (individual curative treatment) or a group when some of a batch is ill (metaphylaxis; Lhermie et al., 2015). In October 2018, the European Parliament ruled against the preventive use of antibiotics, i.e. before the onset of disease, by treating all animals in a batch that has a high probability of a disease occurring. Indeed, their massive use in animal production (Anses, 2020) has contributed to the emergence of resistance that reduces their effectiveness in animals and can be transmitted to humans, either through human-animal proximity or via the food chain. This is why the fight against antibiotic resistance has become a global public health challenge that has been translated into two national action plans (EcoAntibio: 2012-2017 and 2017-2021; https://agriculture.gouv.fr/le-plan-ecoantibio-2-2017-2021)

Monogastric animal species are particularly concerned by these issues. At present, these species are reared mainly in highly organised systems with high animal densities and artificial living environments, and their farms use large amounts of antibiotics (Anses, 2020). In the same issue, Paul et al. (2021) review the evolution of antibiotic use in the monogastric animal sector and present the approaches developed to reduce its use. The objective of this article is to define the principles, develop an analytical framework and identify the practices available at the animal and farming system levels for integrated health management of monogastric animals, mainly pigs, rabbits and poultry. We illustrate this by showing how various practices can be combined to meet this objective and conclude by discussing limitations of current conventional systems and the challenges they must address in pursuit of demedicalisation.

1. Definition and principles of integrated animal health management

2. A conceptual framework for representing animal health

2.1. The components of animal health

To be able to consider the integrated management of monogastric animal health beyond the characteristics of each species, the RIMEL consortium (Fortun-Lamothe et al., 2017) developed a conceptual framework of the components of animal health defined above (Box 1). Its objective is to identify the structural elements that help build up the health of farm animals to integrate it into the knowledge required for integrated management. This framework includes physical and psychosocial dimensions, which are subdivided into 11 components (Figure 1). The physical dimension of health includes physical barriers that interface with the external environment (integument, mucous membranes and microbiota) and the defence system, which consists of the immune, nervous and endocrine systems. The psychosocial dimension includes social connections between individuals (mother-offspring, between congeners), the expression of innate behaviours and respect for the circadian rhythm. These components interact with each other and with the organs involved in major biological functions (section 2.2).

Figure 1. Conceptual framework of the components of animal health.

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Species-specific periods have been identified as critical for health (e.g. perinatal period, weaning) as they correspond to key periods of exposure of animals to high risks at a time when certain components may not have developed completely. For example, most animal species are born with immature immune systems and must rely on maternal immunity (via the yolk, placenta, or milk secretions) in the early stages of life to cope with exposure to multiple biotic and abiotic stressors in the surrounding environment (Brambell, 1970). Similarly, the adaptive immune system of mammals generally does not mature until after weaning (Weström et al., 2020). This event, which involves a change in diet, separation from the mother and sometimes a change in the living environment, represents a risk. The adaptive capacity of young animals can thus be exceeded easily. Even outside these risk periods, health components are influenced by factors intrinsic to the animal (genetics; nutritional, physiological and emotional statuses) which are influenced by the environment (biotic, abiotic and anthropogenic components). These extrinsic factors can positively or negatively influence the building up of health, sometimes in different ways depending on the developmental dynamics of the health components (section 2.3). Integrated health management aims to influence these factors according to Principles 1 and 2 described above and illustrated in section 3. Farmers are not always able to influence certain factors (e.g. climate risks in free-range farming). In these situations, integrated health management implies precaution (e.g. providing shelter) or anticipation as a part of integrated health management.

2.3. A dynamic vision of the building up of health

The DoHAD (Developmental origin of Health And Diseases) concept supports the idea that health is built up in a dynamic process that starts at gametogenesis, including the entire period of foetal and postnatal development, and ends around sexual maturity (Suzuki, 2018). Thus, the parents' living environment influences the health of their offspring through gamete development and the maternal environment during gestation and lactation (Nilsson et al., 2018). For example, dietary restriction in hens influences the immunity of their offspring (Bowling et al., 2018). Similarly, in conventional rabbit farming, rabbits are simultaneously pregnant and lactating. The superposition of lactation and gestation impacts foetal growth (Fortun-Lamothe et al., 1999) and the development of unborn rabbits (Fortun-Lamothe et al., 2000).

Beyond the parental imprint, exposure to favourable or unfavourable situations during development varies among individuals and generates a unique trajectory of strengthening or weakening of health (Figure 2; Halfon et al., 2014). Hertzman and Power (2011) suggested three ways to model effects of the life trajectory on health, two of which are relevant to farm animals. The latent model highlights the relationships between exposure at a given point in life and health years later. In animal production, this model applies to the early programming of phenotypes. For example, the incubation temperature of eggs alters the heat tolerance of chickens (Loyau et al., 2015). In addition, the hours after hatching/birth and the start-up/lactation phase are critical for subsequent health (Guilloteau et al., 2019; Foury et al., 2020). The cumulative model identifies combined effects on health due to multiple exposures throughout the life trajectory. This is the case for pigs, which develop a higher vaccine response when their immunity has been stimulated by hygienic housing conditions (Chatelet et al., 2018). Ultimately, the available knowledge shows that building up an animal's health is an active process involving distinct adaptation mechanisms at different stages of development that coordinate the interactions between all components of an animal's health.

Figure 2. Individual trajectories for building up an animal's health when influenced by events that occur at different stages of the animal's life (adapted from Halfon et al., 2014).

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3. Practices available at the farming system level

3.2. Time frames of practices that can be used in animal production

The practices used for integrated animal health management can act over different time frames (Figure 3). Thus, practices be distinguished by i) direct effects: e.g. feeding protein to piglets around weaning influences their digestive health (Liao, 2021); ii) delayed effects: e.g. egg incubation temperature modifies the heat tolerance of chickens at the end of rearing (Loyau et al., 2015), or the consumption of essential oils during chick start-up permanently modifies the transcriptome of chickens depending on their postnatal experience (Foury et al., 2020) and iii) effects transmitted between generations: supplementing maternal diets of ducks with omega-3 fatty acids can reduce the phenomenon of pecking in the offspring (Baéza et al., 2017).

Figure 3. Time frames of practices that influence animal health: direct effects (A), delayed effects (B) and effects transmitted between generations (C).

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Considering the time frames of practices encourages a long-term vision of animal health management and better understanding of the connections among the systems within the entire production system or between the links in a production chain (breeding stock vs. growing stock; hatchery vs. farm practices). For example, in poultry farming, Van der Waaij et al. (2011) recommend similar rearing conditions for breeders and their offspring. However, in the current broiler industry, breeders are fed a restricted diet to maximise their reproductive performance, while their offspring are fed ad libitum to maximise their growth. Restricting the feed of breeders influences their welfare and immune status (Decuypere et al., 2010) and limits the growth of their offspring (Bowling et al., 2018).

4. Integrating the practices into monogastric animal health in current systems

The practices available at the farming system level for integrated health management of monogastric animals should not be considered separately, but together in an approach of integrated health management. Integration means that practices are coordinated to build up animal health to achieve and/or maintain balance. This includes coordinating practices of prevention and those that develop the adaptive capacity of animals. Conversely, health disorders, when not specific to a pathogen, as in the case of production diseases, are generally multifactorial in origin and occur because several elements combine to exceed the adaptive capacity of the animals (Table 7). In the sections below, we describe how this coordination is performed on pig, poultry and rabbit farms. Note that some of the practices used for their beneficial effects on animal health also help maintain productivity.

5. Limitations of current strategies and ways forward

Generally, over the past few decades, health management on monogastric animal farms has focused on the physical health of the animals and the desire to increase animal productivity for economic reasons. Certain technical choices now cause health and welfare problems (e.g. housing in wire cages and pododermatitis of breeding rabbits). Moreover, these choices have often been made to the detriment of the psychosocial health of the animals (e.g. high animal density, inappropriate living environments and pecking for laying hens; limiting the behavioural repertoire of rabbits reared in cages; stereotypies at the end of pregnancy in sows housed in boxes).

Below, we discuss limitations for pig, rabbit and poultry farms as well as potential strategies for technical development. These limitations are not only technical, but also human and social (need for security, support for new practices, competition for working time), economic (investments, farm profitability) or scientific (genetic selection, early diagnosis of disorders; Ducrot et al., 2018; Piel et al., 2019).

In conventional pig farming, managing piglet health at weaning without using antibiotics remains difficult on some farms. One reason is the age at weaning. European Union Directive 2008/120/EC issued minimum standards for the protection of pigs, which recommends that no piglet should be separated from its mother before it is 28 days old. However, the practice of weaning at 21 days of age has developed strongly in France in recent years to encourage a rapid return to heat and maximise the numerical productivity of sows. Studies in the Americas (Faccin et al., 2020) and Europe (Postma et al., 2017) have shown that a later weaning age (35 days) is associated with lower antibiotic use, probably due to greater maturity of the piglets. Other avenues for progress are mentioned, but they represent significant scientific and technical challenges. They include i) providing forage, which in addition to getting the animals accustomed to solid feed and promoting the development of microbiota, provides a substrate for play, ii) managing sows to promote their welfare during gestation and iii) mixing piglets before weaning to promote social interactions between piglets from different litters (Blavi et al., 2021).

Delaying the weaning age is encouraged in organic farming, which requires weaning after 42 days to approximate natural conditions (90-120 days), and provides interesting avenues for improving piglet health without altering the sows' return to reproduction (Ferchaud et al., unpublished data). Using animals that are resistant to the main pathogens involved in diarrhoea, resilient to weaning, efficient from a feeding viewpoint and adapted to varied and variable rearing conditions would be a major advance (Le Roy et al., 2019). Implementing this depends on scientific advances and changes in breeding programmes. Finally, current housing conditions for lactating sows and piglets are not always conducive to the expression of natural behaviours, positive mother-young relationships, learning to feed or interactions between piglets from different litters. Changing housing systems is often hindered by the economic cost of investment (Bertin and Ramonet, 2016).

In rabbit farming, housing animals in cages with wire mesh floors is justified to manage parasitic infestation by reducing the animals’ contact with their faeces. However, coccidia are present on most conventional farms (protozoa of the genus Eimeria; Licois, 2009) and the use of anticoccidial medicines, mainly robenidine®, remains frequent and is currently causing resistance problems. At the same time, this housing method leads to pododermatitis in breeding females (prevalence: 5-15%; Rosell and De la Fuente, 2013) despite the presence of plastic "leg rest" bottoms. For this reason, rabbit farming is moving towards rearing growing rabbits in pens, often with slatted floors, and in large groups (more than 20 animals). This change leads to more social interactions (at least with conspecifics), which can modify the dynamics of pathogen transmission, especially if animal density is not reduced (currently limited to 45 kg/m² at 70 days of age for growing rabbits). It is thus necessary to reconsider i) the layout of the living environment, to not disrupt these social interactions in relation to animal expectations, and ii) implementation of hygiene and prophylaxis protocols, to reduce pathogen transmission within these large groups. Changing housing could prevent the maintenance of multi-purpose housing for breeding and growing rabbits and lead to abandonment of the “all-full-all-empty” health management currently practised on half of French rabbit farms. This type of management has the advantage of allowing the building and housing to be cleaned and disinfected after each batch of animals. However, it can also promote pathogen transmission because the animals in this confined environment all have the same physiological stage and are therefore exposed to the same degree of risk. Furthermore, as the microbiota influences maturation of the immune system, excessive hygiene could ultimately be detrimental to animal health. Combining animals at different physiological stages is a practice that predates the batch system and should be studied considering the new production methods.

For breeding females, respiratory problems persist despite the methods used to control environmental conditions. Using resistant animals seems to be the most promising approach but remains to be implemented. Furthermore, it has been shown that reducing the rate of reproduction (e.g. insemination every seven weeks instead of the current six weeks) reduces the nutritional demands of the females, which improves their body condition and increases their longevity. Nevertheless, this practice is not widespread and is often restricted to summer for economic reasons (reduction in annual productivity). Finally, individual housing of females is contested by animal rights activists because rabbits are social animals that live in colonies. Group housing of familiar females (biological or milk sisters) is possible until the first kindling (Laclef et al., 2021). After that, however, female rabbits fight and seriously injure each other in an attempt to establish a social hierarchy. A system that is a satisfactory compromise among reproductive performance, health and behavioural expression remains to be found.

In poultry farming, a major limitation to animal health and welfare is the segmentation of the production chain (breeder rearing, hatchery, chicken or pullet rearing, laying house for egg production systems, transport to the slaughterhouse). It leads to waiting and transport phases, especially between the hatchery and the farm, that are a source of considerable stress for the animals. After being handled (sorting and sexing), they are kept without water and feed for several hours and, during transport, may be subjected to variations in temperature and humidity, as well as vibrations and transport hazards. This has been shown to have a lasting effect on their subsequent physical (postnatal hypothermia, altered metabolism, growth retardation; Guilloteau et al., 2019, Beauclercq et al., 2019; Foury et al., 2020) and psychosocial (Hollemans et al., 2018) health. Access to water and feed at hatching is necessary, and they can be provided in hydrated feed at the hatchery and/or in transport boxes or by hatching on-farm (Van de Ven et al., 2011; Leterrier, unpublished data). Furthermore, early implantation of a natural (from or in the presence of adult hens) or selected (gut microflora, probiotics) microbiota barrier reduces the load of salmonella and other enteropathogens (Schneitz, 2005), facilitates maturation of the immune system and helps decrease the mortality rate, which remains high in the start-up phase.

Using highly specialised genetic lines whose metabolism is oriented mainly towards the targeted biological function (growth or egg production) also influences animal health. For example, laying hens that are selected for egg production have a weakened skeleton after 70 weeks. This situation is exacerbated by the rearing conditions, which do not provide the animals with sufficient opportunities to move. In contrast, chickens that are selected for rapid growth and high feed efficiency have pectoral muscle yields greater than 20% but a weakened thermoregulatory capacity (Piestun et al., 2008) and are prone to frequent muscle myopathies such as white streaks, wooden breast or spaghetti muscle (Praud et al., 2020). Using slower-growing lines or mixed lines for both egg and meat production could prevent these disorders.

Finally, feather pecking in laying hens remains a major health problem that is currently managed by modifying the animal's physical integrity (beak trimming). This practice could be avoided by providing fibre-rich feed, enriching the living environment (adapted litter, pecking stones or blocks), genetic selection (control of fear and stress levels) and reducing rearing densities (Rodenburg et al., 2013; Zepp et al., 2018).

6. Future challenges

Currently, some European consumers want animal welfare to be considered better. They do not support practices that modify physical integrity (castration without anaesthesia, tooth grinding, beak trimming, etc.), disapprove of animal production in cages and want animals to be allowed to move freely. Following the citizens' initiative "End the Cage Age" (https://www.endthecageage.eu/), the European Commission has committed to developing a framework for legislative change that would require ending cage farming by the end of 2023 and that would come into force in 2027. Monogastric animal farms are particularly targeted by this initiative (breeding animals and growing rabbits, etc.).

Monogastric animal farming systems will have to change significantly, and health management will have to be re-evaluated accordingly. Improved welfare considerations, however, can sometimes have a negative influence on animal health in these farming systems. This is the case for rabbits (Szendrö et al., 2019) or sows kept in groups. Giving them the opportunity to interact socially with conspecifics results in frequent fighting and a high injury rate until the social hierarchy is established. Research has also shown that although animals with access to the outdoors appear to be subject to fewer respiratory diseases than animals kept in confined systems, they are subject to higher perinatal and reproductive mortality (Delsart et al., 2020). This is due mainly to inadequate control of light and thermal conditions. Health management in these systems should thus include ways to help animals adapt to climate variations (windbreaks, shelter, refuge; Skuce et al., 2013), the ability to predict these variations (access to data or weather alerts) to be able to shelter the animals beforehand and improving the layout of outdoor areas (trees, windbreaks, protective barriers, etc.). Furthermore, animals with access to the outdoors are exposed to more parasites and other infectious agents not encountered in buildings (via feed, soil and contact with wildlife). The layout of the living environment or innovative practices will have to be considered to manage these new challenges. The experiences of farms that comply with organic farming specifications could be valuable (Vaarst and Alroe, 2012). These changes are likely to increase the diversity of farming systems and variability in the health and welfare of animals. These changes are also likely to require more individualised ways to monitor and manage behaviour and health parameters that could benefit from digital applications (Grosse-Kleimann et al., 2021).

Conclusion

Animal health, which is both a state and a process, is built up throughout an animal’s life. In pig, rabbit and poultry farming, many practices are available and must be used consistently in an approach of integrated animal health management. Their main objective is to promote health, prevent contact with harmful biotic and abiotic elements, and support the adaptive capacity of animals so they become tolerant of these elements. However, antibiotics and antiparasitic agents are still used on these farms. This situation is due mainly to technical or organisational choices that are motivated by economic reasons, which lead to situations that exceed the animals' capacity to adapt. This is the case in pig farming, in which the digestive and immune immaturity of piglets at weaning is a risk factor for digestive disorders. This is also the case in poultry farming, in which the conditions under which the animals are transported from the hatchery to the farm generate stress that has a lasting effect on their health, and in which genetic selection that is oriented toward production weakens their ability to adapt.

Some of these choices, especially those related to housing, are currently criticised by society for not respecting animal welfare. These criticisms are driving the emergence of new farming systems that raise new questions about animal health. Animals' access to the outdoors also modifies the boundaries and dynamics of flows (matter, xenobiotics, pathogens, individuals, genes) between animals and wildlife and between animals and highly human-modified environments. In reference to the "One Health" concept, greater proximity of animals to vectors, pathogen reservoirs or xenobiotics in the wild or to human-modified environments represents a challenge for integrated health management (Esther et al., 2016).

Acknowledgements

The authors thank Catherine Schouler for her contribution to the reflections and her proofreading, Cécile Berri for her expert contribution on avian muscle disorders and Agnès Girard for her help with bibliographic research.

The manuscript was translated by DeepL and proofread by Mme Corson.

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