INTRODUCTION

There is growing recognition that industrial livestock production, in which large numbers of animals are kept in crowded and stressful conditions, can lead to the emergence, transmission, and amplification of both viral and bacterial diseases, some of which are zoonotic. A Joint Scientific Opinion by the European Medicines Agency (EMA) and the European Food Safety Authority (EFSA) states that “the stress associated with intensive, indoor, large scale production may lead to an increased risk of livestock contracting disease” [1].

The report Preventing the next pandemic by the United Nations Environment Programme and the International Livestock Research Institute identifies unsustainable agricultural intensification and increasing demand for animal protein as major drivers of zoonotic disease emergence [2].

A key study collected samples from nearly 2500 European pig holdings [3]. Many of the samples were from “regions of very intense pork production in Europe.” The study found a year-round presence of up to four major swine influenza A virus lineages on more than 50% of the farms surveilled. The authors conclude that “European swine populations represent reservoirs for emerging IAV [influenza A virus] strains with zoonotic and, possibly, pre-pandemic potential.” The paper's highlights state that “European swine populations host building blocks of pre-pandemic influenza viruses.”

A 2022 study states: “Large pig and poultry farms are where the genetic reassortment needed to source pandemic influenza strains may most likely occur” [4]. A report by the International Union for Conservation of Nature states that: “The global trend in large scale industrial production of pigs, poultry and farmed-wildlife species is coincident with pandemic emergence of highly pathogenic human or zoonotic influenzas, and coronaviruses” [5]. It adds: “A certain way to reduce risk of zoonosis and emerging infectious diseases globally … is to reduce dependence on intensive animal-based food production systems.”

A recent study points out that “intensive animal farming creates conditions for the emergence and amplification of epidemics because of the physical and genetic proximity of the billions of animals, often in frail health, that are raised indoors every year” [6].

Industrial farming can also have an indirect effect on the emergence of new viruses. Industrial animal agriculture needs huge amounts of soy and cereals to feed the animals. This leads to the expansion of farmland into forests and other wildlife habitats. This results in ecosystem disruption and loss of biodiversity, both of which increase the risk of pathogen spillover [6, 7]. A study published in Nature reports that human encroachment into natural habitats, for example, through agricultural expansion, can lead to an increased risk of zoonoses [8]. The study found that the expansion of human activities into forests and grasslands leads to the decline of some species, whereas others thrive. The losers tend to be ecological specialists, such as rhinoceros or ostriches, who have highly specific feeding or habitat requirements and who are comparatively larger than nonspecialists. The winners are often generalists who are small and abundant and who have “fast, short lives,” such as rats and starlings. The researchers report that these winners are much more likely to harbor pathogens than the losers. As a result, when we convert natural habitats to our own uses, we inadvertently increase the probability of transmission of zoonotic infectious diseases. These factors, together with closer contact between people, such as farm workers, and wildlife can lead to viruses being transmitted from wild animals to people [9].

WHY BIOSECURITY IS NOT ON ITS OWN SUFFICIENT

Effective biosecurity is of course essential to minimize disease risks. However, it cannot be totally successful in excluding pathogens.

In a 2021 report on avian influenza, the EFSA said: “The frequent occurrence of HPAI A(H5) virus incursions in commercial farms where birds are kept indoors including poultry production types considered at low avian influenza risk (e.g. broilers and breeders) raises concern about the capacity of applied biosecurity measures to prevent virus introduction” [10].

Similarly in a 2022 report, the EFSA said: “outbreaks often occurred in establishments without outdoor access, and poultry production systems (e.g. breeders) with high biosecurity standards were also affected” [11].

In the same report, the EFSA added: “The biosecurity measures implemented along the poultry production chain do not seem effective in preventing all introductions of the HPAI A(H5N1) virus into poultry establishments.”

A recent study points out that intensive animal production reduces the risk of contact between farmed animals and wild animals and pathogens [6]. The study states that intensified farming has probably reduced the likelihood of disease entering farms through contact with wild animals but has worsened the consequences of disease when it does enter the farm. The authors point out that disease “events may have become less frequent but are far more severe.” They explain that “high animal density in intensive farms leads to a greater spread of pathogens within the facilities. Thousands of animals can be infected within a few days. Second, the selection of the most profitable species of farmed animals in intensive farms has led to a high level of genetic similarity. The genetic similarity among farmed animals facilitates the spread of the pathogens … increasing the chance of catastrophic epidemics. In addition, genetic proximity and high density together offer ideal circumstances for the pathogens to mutate and evolve, which increases the risks of a mutation that is transmissible to humans.”

HIGH ROUTINE PREVENTIVE USE OF ANTIMICROBIALS IN INDUSTRIAL LIVESTOCK PRODUCTION

A key approach taken by the industrial livestock sector to reduce the incidence of bacterial disease is to routinely include antimicrobials in the feed or water of animals to prevent disease.

Over 70% of global use of antimicrobials is in animals [12], and most of this use is to prevent disease or promote growth. This high use of antimicrobials contributes significantly to the emergence of bacteria that are resistant to antimicrobials. These bacteria may be resistant not only to antimicrobials used in farming but may also develop resistance to related antimicrobials used to treat serious human disease.

The World Health Organization (WHO) states: “Extensive research into mechanisms of antimicrobial resistance, including the important role of horizontal gene transfer of antimicrobial resistance determinants, supports the conclusion that using antimicrobials in food producing animals selects for antimicrobial resistance in bacteria isolated from food producing animals, which then spread among food-producing animals, into their environment, and to humans” [13].

The O’Neill Review on Antimicrobial Resistance, established by the UK Government, reports a clear link in the scientific literature between antimicrobial consumption in farm animals and resistance in humans. It calls for a substantial reduction in antimicrobial use in farming as an important aspect of the strategy for combating antimicrobial resistance [14]. WHO Guidelines recommend: “an overall reduction in use of all classes of medically important antimicrobials in food-producing animals” [13].

ROUTINE PREVENTIVE USE OF ANTIMICROBIALS IS PRIMARILY A FEATURE OF INTENSIVE LIVESTOCK PRODUCTION

The EMA has said: “In animal production systems with high density of animals or poor biosecurity, development and spread of infectious diseases is favored, which leads more frequently to antimicrobial treatment and prevention of those diseases. This provides favorable conditions for selection, spread and persistence of antimicrobial-resistant bacteria. Some of these bacteria are capable of causing infections in animals and if zoonotic also in humans. Bacteria of animal origin can also be a source for transmission of resistance genes to human and animal pathogens” [15].

The O’Neill Review on Antimicrobial Resistance mentioned above states that prophylactic use is “particularly prevalent in intensive agriculture, where animals are kept in confined conditions” [14].

The WHO states growing demand for meat “especially when met by intensive farming practices, contributes to the massive use of antibiotics in livestock production” [16].

The UN Food and Agriculture Organization states: “the prevalence of resistance in the agricultural sector is generally higher in animal species reared under intensive production systems” [17].

It is increasingly being recognized that the proper way to avoid illness in farm animals is to keep them in good conditions rather than to routinely include antimicrobials in the feed and water of animals to prevent disease.

PREVENTING DISEASE WITHOUT REGULAR PROPHYLACTIC USE OF ANTIMICROBIALS: DEVELOPING HEALTH-ORIENTED SYSTEMS FOR REARING ANIMALS

There is broad agreement that improved husbandry would reduce the risk of disease. The Federation of Veterinarians of Europe states: “animals that are well cared for and appropriately housed, will experience a better welfare, be less prone to infections and will need fewer antibiotics.” It adds that “a positive association can be seen often between good animal welfare and reduced antibiotic use. In other words, the more successful the actions aiming at improving animal health and welfare are, the more successful will be the attempts to reduce the use of antibiotics and to curb bacterial resistance in food animals” (emphasis present in the original) [18].

The Joint Scientific Opinion by the EMA and the EFSA referred to earlier recommended options that include “improving husbandry and management procedures for disease prevention and control; rethinking livestock production systems to reduce inherent disease risk.” It states: “measures must be implemented that improve animal health and welfare and thereby reduce the need for antimicrobials in the first place.”

The Joint Scientific Opinion examines the factors needed to create more resilient animals that are less susceptible to disease. It states that these include reducing the level of stress resulting from factors such as heat, cold, crowding, restraint, mixing, early weaning, feed restriction, insufficient bedding, lack of enrichment, and noise. It adds: “crowding and restraint put pressure on animals.” Many of these factors are most typically found in industrial livestock systems. It concludes: “On-farm stressors interfere with the normal behavior of the animals and have been shown to alter the immune system of animals and susceptibility to diseases.”

The Joint Scientific Opinion highlights the “need to rethink those particular farming systems which place much reliance on antimicrobial use.” It states: “In some farming systems, much reliance is placed on the routine use of antimicrobials for disease prevention or for the treatment of avoidable outbreaks of disease, such that these systems would be unsustainable in the absence of antimicrobials.” It recommends: “Farming systems with heavy antimicrobial use should be critically reviewed, to determine whether/how such systems could sustainably reduce the use of on-farm antimicrobials. If a sustainable reduction in the use of on-farm antimicrobials is not achievable, these systems ideally [should] be phased out” [19].

The Lancet Infectious Diseases Commission has stressed that instead of relying on routine use of antimicrobials, we need to develop “health-orientated systems for rearing of animals” [20]. In such systems, good health would be integral to the system rather than being propped up by routine use of antimicrobials. This approach would build good health and strong immunity by addressing the following factors:

Avoiding overcrowding: Research shows that high densities are a risk factor for the spread and development of infectious disease; such densities can allow rapid selection and amplification of pathogens [21-23]. The European Commission's Guidelines for the prudent use of antimicrobials in human health highlight the need to “reduce the density of the farm animal population” saying “this is believed to be a major risk factor in the emergence and spread of infections” [24].

To the best of my knowledge, no studies have investigated what maximum stocking densities should be in order to minimize disease risks. However, the EFSA has recently recommended maximum stocking densities for broilers (chickens reared for meat), egg laying hens, and pigs. The EFSA was considering stocking densities from an animal welfare viewpoint but as indicated earlier, animal welfare, animal health, and disease risk are closely connected.

To produce its Scientific Opinions, the EFSA carries out an extensive review of all scientific studies regarding a particular species. In its 2023 Scientific Opinion on broilers, the EFSA recommended that a “maximum stocking density of 11 kg/m² should be applied to allow the broilers to express natural behavior, to rest properly and to support health” [25]. Their opinion states: “The maximal stocking density above which FPD [footpad dermatitis] score will increase, walking ability will be reduced and behavioral needs realization is impaired because of lack of space is 11 kg/m².”

These factors relate to disease as well as welfare. Inability to perform natural behaviors is stressful, and stress can weaken immune competence. The EFSA points out that footpad dermatitis can entail soft tissue lesions and integument damage and can involve inflammatory states in the subcutaneous tissue leading to hyperkeratosis, necrosis, and ulcerations [25].

In its 2023 Scientific Opinion on the welfare of laying hens, the EFSA stated that hens should not be kept in cages and recommended a maximum stocking density in barns of four laying hens/m² (this equates to 2500 cm²/bird) to minimize soft tissue and integument damage and “reduce the risk of plumage damage and allow unconstrained performance of motivated behaviors, including those that occupy most space (e.g. wing flapping)” [26].

In a 2022 report on the welfare of pigs, the EFSA recommends the minimum space allowances set out in the first column of Table 1 where ambient temperatures do not exceed 25°C [27]. The EFSA states that these space allowances are needed to maintain separate dunging and lying areas and that at these allowances the growth rate is less compromised and tail biting is reduced.

The EFSA recommends that at temperatures above 25°C and for pigs weighing above 110 kg (even when the temperature is below 25°C), the space allowances set out in the second column of Table 1 should be provided as these will enable lateral lying, that is, lying separately on their sides with legs extended. The ability to lie laterally is essential at high temperatures to reduce the risk of heat stress. The EFSA states that at these higher space allowances, the growth rate is even less compromised.

The EFSA recommended these space allowances from the viewpoint of improving animal welfare and the growth rate. Nonetheless, they may also be a helpful starting point for considering the vulnerability of pigs to contract diseases at different stocking densities.

Reducing stress: Stress tends to impair immune competence, making animals more susceptible to disease [19, 28]. The Joint EMA/EFSA Scientific Opinion states that the following steps contribute to reducing stress: the provision of proper enrichment, ensuring thermal comfort, proper animal handling, and avoiding feed restrictions. The Joint Opinion points out that pregnant sows and broiler breeders are regularly feed restricted. Martínez-Miró et al. (2016) state: “In stressful situations there may be a reduction in the normal function of the immune system …This will result in an increase in the presence of diseases” [29].

Enabling animals to perform natural behaviors: Inability to engage in natural behaviors is a major source of stress in intensive systems [19]. Martínez-Miró et al. write: “the barren environments of modern production systems have a negative effect on animal welfare due to the lack of bedding material and/or slatted pen floors. They create a poor environment where pigs cannot develop their natural behavior. Inability to perform highly motivated behaviors may lead to a stress response” [29].

Ending the early weaning of pigs: Under natural conditions, weaning is a gradual process, which is not completed until 13–17 weeks of age [27]. Farmed pigs are often weaned at 21–24 days of age or even at a younger age.

Such early weaning is stressful due to premature and abrupt separation from the sow, change in diets, mixing with unfamiliar pigs from other litters, and being moved to a new environment [30].

When abruptly removed from the sow's milk, there is a sharp decrease in nutrient intake while the piglet learns to eat and digest solid food. This can lead to prolonged hunger for the piglet [27]. Since milk also supplied much of the fluid intake prior to weaning, piglets may experience prolonged thirst as they get used to the water delivery system provided after weaning.

However, more long-lasting consequences of the postweaning period of undernutrition are detrimental changes in intestinal morphology and the gut microflora. The EFSA states that these changes “impair nutrient absorption, compromise gut integrity, and allow proliferation of pathogenic organisms within the gut which can produce toxins migrating to the bloodstream and exerting systemic effects. This situation is exacerbated by the withdrawal of local protective effects within the gut of immune proteins present in maternal milk, and by the immaturity of the piglet's systemic immune system. Passive immunity obtained from ingestion of colostrum wanes progressively from the first to the sixth week of life, while the piglet's own ability to mount an active immune response develops only gradually during and after this time. The combined effect of these challenges means that piglets weaned at a young age are highly susceptible to health disorders, and particularly gastro-enteric disorders” [27].

To avoid the above problems, pigs should not be weaned until they have gained immunological and nutritional independence from sows.

The detrimental impacts of early weaning on pigs' health are highlighted by the much higher use of antimicrobials in early weaned piglets than in those weaned at a later age. The Danish Ministry of Agriculture data show that antimicrobial use is 20 times greater in intensive weaners than in organic pigs that are weaned at a substantially older age [31].

Pigs should at the earliest be weaned at 28 days of age and preferably later [31]. Research shows that weaning at 22–25 days of age, which is common in pig farming, results in 15–20 times higher use of antimicrobials than later weaning at around 35 days of age or more [32, 33].

Avoiding excessive group size: The O′ Neill Review states: “large numbers of animals living in close proximity … can act as a reservoir of [antimicrobial] resistance and accelerate its spread. There are often many opportunities in intensive farming environments for drug-resistant bacteria to be transferred between, for example, thousands of chickens being reared in the same indoor enclosure” [34].

Meadows et al. (2018) state that their study was able to “clearly demonstrate the increase in epidemic size that occurred as farm sizes grew larger.” They suggest that “livestock production trends in many industrialized countries that concentrate livestock on fewer, but larger farms have the potential to facilitate larger livestock epidemics” [35].

Minimizing mixing: Mixing is stressful and can result in the introduction of disease [24].

Maintaining good air quality: Poor air quality such as high levels of ammonia and airborne dust together with inadequate ventilation are risk factors for respiratory disease [24, 36, 37].

Encouraging a move away from genetic selection for high production levels as these appear to involve an increased risk of immunological problems and pathologies [38]. Genetic selection for fast growth, high yields, and large litters has placed considerable pressure on the health of farm animals and in this weakened state, they may be more vulnerable to disease.

Broiler chickens: Traditionally meat chickens—broilers—would take around 84 days to reach their slaughter weight of 2 kg. However, today's broilers have been selectively bred to often reach a slaughter weight of 2.2 kg in 35–38 days [39]. Modern broilers are growing twice as quickly as 60 years ago [40].

What grows quickly is the muscle—the meat. But the supporting structure of the legs, heart, and circulatory system cannot keep pace with the rapidly growing body and cannot properly support it. As a result, each year, globally, billions of broilers suffer from painful leg disorders, while others succumb to heart disease [41, 42]. Moreover, compared with slow growing birds, fast-growing broilers have higher levels of breast muscle disorders and hock burn [43-45].

The poor health of fast growing broilers is highlighted by Dutch data showing that standard fast-growing chickens receive substantially more antimicrobials per bird than slower-growing breeds [46, 47].

Laying hens: The Red Jungle Fowl—the wild birds from whom today's laying hens are descended—lay about 20 eggs per year [48]. But today's hens produce over 300 eggs a year.

A report by the UK Farm Animal Welfare Council, an independent body that advises the government, concludes that genetic selection for high egg yields causes osteoporosis and results in hens being very vulnerable to bone fractures [49]. Their report adds that it is questionable whether it is possible to maintain an egg output of around 300 eggs in the laying cycle while attaining bone strength sufficient to reduce this vulnerability to bone fractures.

Sandilands (2017) states that today's high yielding hens are “continuously depleting calcium from their bones” and that they “halve their cancellous bone volume between 16 and 31 weeks of age” [50].

A 2021 Danish study reports that around 85% of Danish laying hens suffer from keel bone fractures [51]. The fractures appear to be the result of disproportionately large eggs in hens that are too small for such eggs. This seems to be the result of breeding strategies that aim at smaller hens with a low food intake, and at the same time, high egg production with an early start of lay and large eggs. The large eggs apparently pressurize the hens' bodies from within.

Dairy cows: A cow producing just enough milk for her calf would produce just over 1000 L in her 10-month lactation. But commercial dairy cows have been selected for much higher yields; many dairy cows are now producing 10,000 L a year [52]—in some cases 12,000 L a year.

A review of the scientific literature concluded that “genetic selection for high milk yield is the major factor causing poor welfare, in particular health problems, in dairy cows” [53]. The review added: “The genetic component underlying milk yield has also been found to be positively correlated with the incidence of lameness, mastitis, reproductive disorders and metabolic disorders.”

A report produced by Professor Donald Broom, Emeritus Professor of Animal Welfare at Cambridge University, states: “Dairy cows producing large quantities of milk have high levels of leg disorders, mastitis and reproductive disorders. The proportion of cows affected by one or more of these disorders is high and the animals live with the poor welfare for a substantial part of their lives” [54].

Pigs: Large litter size is recognized as a significant cause of multiple welfare problems for both sows and piglets [55]. Piglet mortality increases with increasing litter size due to low birth weights, variability in piglet weights, a greater percentage of low viability piglets, an increased proportion of crushed piglets, and starvation caused by some piglets being unable to access a teat [56-58]. When litter size is large, sows are at a greater risk of losing body condition, increased recumbency, and more shoulder sores [55].

CONCLUSION

Industrial livestock production represents a major threat to both animal and human health. Keeping large numbers of animals in crowded stressful conditions contributes to the emergence, transmission, and amplification of pathogens including zoonoses, some of which have the potential to cause pandemics. Biosecurity is not sufficient on its own to prevent the introduction of disease; it must be combined with keeping animals in conditions that minimize the major drivers of disease.

Industrial livestock production is dependent on the routine use of antimicrobials to prevent the diseases that are inevitable when animals are kept in poor conditions. This leads to the emergence of antimicrobial resistance, thereby undermining some of the key medicines on which human health depends. We need to move to health-oriented systems in which good health is inherent in the farming methods rather than being propped up by routine use of antimicrobials.

AUTHOR CONTRIBUTIONS

Peter Stevenson: Conceptualization (lead); data curation (lead); formal analysis (lead); funding acquisition (lead); investigation (lead); methodology (lead); project administration (lead); resources (lead); software (lead); supervision (lead); validation (lead); visualization (lead); writing—original draft (lead); and writing—review and editing (lead).

CONFLICT OF INTEREST STATEMENT

The author declares no conflicts of interest.