Introduction

In the beginning of August 2007, foot and mouth disease (FMD) was confirmed on a cattle holding near Guildford in Surrey (United Kingdom, UK) and shortly afterwards on a second nearby site. The day after the first outbreak a UK wide ban on all livestock transport was in place [4, 18]. A few days later the European Commission decided that no live animals susceptible to foot and mouth disease (cattle, sheep, goats and pigs), or products from these animals, could be transported from or to Great Britain [12]. Except for the 10 km zone surrounding the affected holdings, this ban was lifted at the end of August 2007. Many feared a replay of the 2001 foot and mouth disease outbreak in the UK that lasted for over 6 months and led to the destruction of about four million animals including three million sheep, 600,000 cattle and 138,000 pigs.

The 2001 foot and mouth disease epidemic in the UK cost the national treasury £2.7 billion including £1.2 billion compensation paid to farmers for animals culled under control measures, £701 million spent on eradication measures and £471 million compensation for animals killed for welfare reasons [14]. Although livestock producers are often the first to be affected by disease outbreaks, epidemic disease outbreaks costs can be extensive in the intensively organized livestock production systems. Generally, costs can be divided into direct disease control cost (labor, materials, services, transport and disposal), cull compensation costs, uncompensated industry costs (withholding costs, loss of quality, auction markets and abattoir losses, culling for welfare reasons and export losses) and wider economic costs (tourism, loss of amenity, environmental impact and wider economic effects) [17]. As an example, the total cost of the 2001 foot and mouth disease outbreak in the UK is estimated at £9 billion [16]. Apart from foot and mouth disease, the European Union (EU) has witnessed other important epizootics (animal diseases such as bluetongue, BT, that affect only non-human animals) and zoonoses (diseases such as Bovine Spongiform Encephalopathy, BSE, and highly pathogenic avian influenza, HPAI, which are also contagious for humans). These disease outbreaks had substantial economic and market impact, human health risks, animal suffering and consumer trust issues. Questions were raised about the moral justification of massive culling of infected and healthy animals, as well.

Current diagnosis strategies mainly focus on passive surveillance where the veterinary authorities rely solely on the identification, investigation and mandatory reporting of clinical suspects by livestock producers, veterinarians and others involved in handling livestock. For this system to function effectively, several factors such as disease awareness and willingness to report must be considered [19, 28]. Disease awareness can be difficult to attain, especially if the disease is slow-spreading (e.g. BSE) and has a low prevalence and an incubation period close to the productive lifetime. The willingness to report suspected cases is highest when the negative economic impact and social stigma upon a positively identified case are minimal. The main sources of diagnostic uncertainty are failure of stockpersons and/or veterinary surgeons to notify, adequately interpret disease symptoms and exclude diseases with similar symptoms, variation in clinical signs and inappropriate specimen collection from suspect clinical cases [5]. In practice, this passive surveillance system fails to respond adequately to fast spreading diseases and disease management to tackle fast spreading of disease outbreaks is significantly delayed. As a result, infectious agents of most (highly) contagious diseases are spread before symptoms of the infection occur.

Active surveillance involves the targeted screening of animals towards a specific disease and can be post-mortem or ante-mortem. For example, to safeguard the consumer food chain, since 2001 in the European Union all cattle over 30 months for human consumption is tested post-mortem for BSE [11]. Obviously, this implies a significant economic burden on the cattle sector and government finances.

Nano-enabled diagnostics could be a technological answer to enhance active surveillance with more ante-mortem diagnostic information. These devices contain one or more biosensors with nanosized components (1 nm is one billionth of a meter). The devices themselves can be in the nano or micro range, or even larger. If these miniaturized devices are implanted, they can be extremely useful in delivering real-time information about the health status of animals. A biosensor is a device that consists of a biological recognition system, often called a bioreceptor (an enzyme, a DNA strand, an antibody, a cell or part of a cell) and a transducer [61]. The interaction of the analyte with the bioreceptor is designed to produce an effect measured by the transducer, which converts the information into a measurable effect, such as an electrical signal [60]. Nanobiotechnology is the convergence of engineering and molecular biology and is leading to a new class of multifunctional devices for biological and chemical analysis with better sensitivity, specificity and a higher rate of recognition [24].

This paper consists of two main parts: a technical discussion on disease outbreak management, epidemics and biosensors and an ethical discussion on the impact of nano-enabled diagnostics. The technical discussion is not intended to provide a complete overview of all disease characteristics of BSE, foot and mouth disease, avian influenza and bluetongue. Up-to-date knowledge can be consulted on the website of the ‘Office International des Epizooties’ or OIE (www.oie.int). Rather, the paper aims to illustrate the diversity and complexity of livestock surveillance and disease management. The ethical discussion offers a first overview of relevant ethical issues when nano-enabled diagnostics are to become implemented in livestock production. It elaborates on the experiences in biomedical ethics and indicates the similarities and differences. The main ethical points of this paper could be seen as applicable, at least, to all member countries of the OIE.

Disease Outbreak Management

Disease outbreak management is often very complex because no new disease outbreak is identical to the previous one(s) and many variables interfere with the final outcome. It requires that detailed contingency plansFootnote 1 are developed and updated in tempore non suspecto but especially efforts, inventiveness and experiences in the confusion of an outbreak. An official outbreak meets one or more of the following criteria [10]:

the observation of clinical signs in an animal of a susceptible species consistent with the disease, the isolation of an infectious agent from an animal or derivate, or the antigen detection and identification specific to one or more serotypes of samples collected from animals of susceptible species.

The term ‘epidemic disease’ is used to indicate that there is an unexpected and substantial increase in the number of cases of an infectious disease in a population. An endemic disease on the other hand is commonly present in a population although the incidence rate may vary. The same disease can be endemic in some regions but epidemic in others or its status may change from epidemic status to endemic [29]. The latter can be illustrated by bluetongue. The bluetongue virus has long been present in a broad range of countries extending approximately between 35° S and 40° N. In 1998 it started its invasion in Europe, it crossed the Mediterranean Sea and since then sporadic outbreaks have been reported more northwards [35]. In 2006, it was first recorded in more northern regions such as Belgium, The Netherlands, Germany and Northern France. This northward expansion is speculated to be facilitated by changes in European climate zones by global warming with increased virus persistence during winter [46].

In order to protect trade, current animal production focuses on creating a disease-free status of a country. But as a result of globalization and intensification of production methods, it requires continuous efforts to maintain this status. Therefore, the OIE, also known as the World Organization for Animal Health, tries to harmonise the methods and protocols for the surveillance and control of the most important diseases worldwide.Footnote 2 , Footnote 3 The OIE has set up a list of notifiable diseases including BSE, foot and mouth disease, highly pathogenic avian influenza and bluetongue. This list contains contagious diseases which may have significant socio-economic consequences and/or may impose human health risk and replaces the previous OIE list A and list B. The OIE Manual describes the protocols of reference tests and should be adopted by national laboratories.

The main strategies in the ‘disease-free status’ management are prevention and eradication. Prevention refers to the whole of measures by reducing the risk of disease introduction. Eradication means the complete elimination of the disease and may involve stamping out, vaccination or a combination of the two [58]. A 2004 socio-ethical survey, with a selection of stakeholders involved in livestock production or the decision making-process from every EU member state, showed that a majority defined efficiency to successfully eradicate a disease as the most relevant issue in control strategy and, in general, preventive measures were preferred [13].

Disease Information

The gathering and interpretation of epidemiological data are essential as they cover the vital information of a disease. The importance and suitability of nano-enabled diagnostics will depend on some generic and specific characteristics of these diseases. Table 1 summarizes the impact of outbreaks of BSE, foot and mouth disease, highly pathogenic avian influenza and bluetongue on economics, human health and animal welfare. This evaluation is not absolute but gives a tentative assessment of the variation in impact for a country like Belgium (high cattle, pig and poultry density, low sheep density).

Table 1 Impact of four animal disease outbreaks on economics, human health and animal welfare in Belgium
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Bovine Spongiform Encephalopathy or BSE is a disease characterized by the accumulation of prions (proteinacious infectious particles) and the vacuolation of the central nerve system in the final stages of the disease [20]. There is evidence of a causal link between the BSE agent and a new variant form of the human Transmissible Spongiform Encephalopathy (TSE), Creutzfeldt–Jakob Disease (vCJD).Footnote 4 The nature of the agent causing the TSE is still unknown. According to current knowledge, a disease-specific form of a membrane protein PrP (PrPres; PrP: Prion protein) has a critical importance in the pathogenesis of TSE diseases and the disease agent does not contain polynucleotide [49]. At present, there are no diagnostic tests for the BSE agent in the live animal and the demonstration of the morphological features of spongiform encephalopathy has to occur by histopathological examination [42]. But recently, an important step has been taken to the development of the detection of prions in blood from infected animals during the presymptomatic phase as well as detection of PrPSc in plasma and other blood fractions [9].

Foot and mouth disease is a highly contagious, but rarely fatal disease for cattle, pigs, sheep and goats with important loss of production in the longer term. The foot and mouth disease virus belongs to the Picornaviridae family of viruses with seven distinct serological types of FMD and can not be differentiated clinically from other vesicular diseases. Laboratory diagnosis of any suspected foot and mouth disease case is therefore a matter of urgency [32].

Highly pathogenic avian influenza belongs to the influenza A virus family and results in disastrous effects on poultry productivity and high mortality. It may interfere with human influenza viruses resulting in the potential emergence of a new virus and a potential new influenza pandemic [8, 27].

Bluetongue is an insect-borne, viral disease of ruminants and contains more than 24 serotypes. The BT virus is transmitted by the Culicoides midges and the outcome of infection ranges from very mild in the vast majority of infected animals to fatal in a proportion of infected sheep and goats. Although cattle and goats usually show no clinical signs of the BT infection, they can be a carrier. It is not contagious for humans. The lack of effective sanitary treatment focuses preventive and control measures on vector control in disease-free and infected areas, movement restriction of live ruminants from affected to non-infected areas, symptomatic treatment and vaccine development [22]. Animals from infected areas can be transported to infected areas in the same country or other EU member states as long as they do not show clinical signs of BT, with proper certificates and appropriate biocide treatment [23].

Stamping Out Procedures

Stamping out involves the partial or complete depopulation of infected holding(s) by the culling of susceptible animals, followed by the disposal of carcasses and potential risk goods and the decontamination of holdings and increased surveillance in the surroundings of the infected holdings. This depopulation procedure is applied to deny an infectious agent access to other susceptible hosts.

In general, countries confronted with an epidemic disease outbreak deploy stamping out as the main control and eradication strategy. By using this strategy they hope to regain the profits from a disease-free status, recognized by the OIE, as fast as possible.Footnote 5 However, stamping out does not have to be the standard eradication strategy for all disease outbreaks [58]. Depending on the seriousness of the epidemic, it may include ‘ring-fencing’, i.e. the installation of a protection zone around infected farms with pre-emptive culling and a surveillance zone with a regional or national stand still of transport, and an export stop. The protection zone is characterized with the most restriction measures such as the prohibition of movement and transport of animals of susceptible species, the registration of all holdings with animals of susceptible species, the registration of all stocks of derivates and periodical veterinary inspection and extended sanitary measures (such as cleansing and disinfection) for humans and their equipment. Hence, stamping out constitutes a whole chain of measures of eradication and containment that come into place when an animal disease outbreak occurs. In the EU, additional criteria and risk factors can be specified to determine whether or not depopulation of holdings is appropriate in restricted zones (e.g. Annex IV of the EU Directive 2005/94/EC for avian influenza).

One of the many ethical issues at stake in the context of animal disease control is animal welfare [2]. For evident reasons, welfare is threatened by the disease itself. Prevention should therefore be a central element in any animal disease management strategy. Unfortunately, even with the best prevention methods, a disease outbreak might still occur. If the decision is taken to install control (or even eradication) measures, there are a number of ways in which animal welfare can be violated.

During an epizootic event, the main focus is on getting the control measures in place as quickly, thoroughly and efficiently as possible. For instance, transport restrictions have to be enforced strictly where necessary and culling and destruction needs to be done fast and safely. All these reasons can lead to situations in which animals are treated in ways that seem ethically unacceptable. The OIE has issued a lengthy document containing guidelines describing rather general principles concerning qualification of people involved in culling, operational procedures, welfare aspects and a summary of available methods [51]. For example, in the case of poultry, at least eight general killing methods are mentioned: non-penetrating captive bolt, maceration, electrical killing, CO2/air mixtures, CO2/N2 or inert gas mixtures, N2/inert gas mixtures, lethal injections and feed/water additives. Of these, only electrical and gaseous killing methods are deemed useful for on-farm killing of poultry during an animal disease outbreak. Although these methods have been identified as applicable for the killing of poultry during a disease outbreak, often little published and/or peer-reviewed information is available. Possible welfare problems associated with culling are as diverse as the techniques themselves and range from overcrowding over abuse during handling, to pain caused by insufficient stunning.

Alternative Eradication Strategies to Stamping Out

Other disease control measures include vaccination and a combination of vaccination and stamping out. Vaccination can be used in various ways depending on the time of application or the spatial organization of the vaccination. Preventive vaccination is applied in advance to the actual disease outbreak, while emergency vaccination is applied during the disease outbreak in order to limit the disease spread. Routine vaccination is the consequent vaccination in a certain frequency of all livestock, while target vaccination is limited to certain high-risk groups [58]. Ring vaccination is an emergency procedure which aims to create an immune belt around infected farms, while blanket vaccination involves the vaccination of all susceptible animals over a larger area. It may be the preferred option when the disease outbreak has become well established and when there are multiple sites of infection, or when other disease control methods are impractical for one reason or another [26].

All types of vaccination involve the application of dead or seriously weakened agents. By exposing animals to these agents, they develop an immunological reaction to the real agent. Several important factors determine the effectiveness of the vaccination strategy [26]: vaccine type, quality, protection, storage, application, and vaccination coverage.

Vaccination programs may be the strategy of choice in areas where large-scale stamping out eradication is unacceptable for economic, ethical or cultural reasons. Compared to culling alone, vaccination can have several benefits such as a lower number of animals culled for disease control, unless they are rejected on the market and as a result culled for trade reasons [17].

Public Consequences of Stamping Out and Vaccination

Stamping Out

The stamping out strategy presupposes that the killing of animals is morally justified. This moral justification is grounded on a utilitarian basis; proponents of this strategy argue that an amount of animals is culled as a sacrifice to avoid the total loss of a region’s or nation’s susceptible livestock. It is the safest method in the sense that it can be applied to many infectious diseases, while alternatives such as vaccination are not always available. But many perceive the culling of animals, even if it is done with respect to animal welfare regulations, as an infringement of animal welfare on a large scale that is disproportional with the achieved goals and therefore not acceptable. The death of a farm animal for other reasons than for food consumption is perceived not only as a loss of effort and money but also as a loss of functional determinacy, i.e. the primary function of a farm animal to provide quality food, was not fulfilled [53].

Economic and veterinary arguments by themselves provide insufficient grounds to justify non-vaccination, movement restrictions and massive culling of healthy animals [13]. The policy of ‘ring fencing’ around each outbreak with scheduled culling of potentially still healthy animals in particular, has received a lot of criticism and hostility [36]. The proportion of culled infected animals to culled healthy animals can be very low, especially in animal-dense regions. For example, in Belgium and The Netherlands a total of 4.1 million and 30.3 million birds were culled [21, 54]. Of that number, in the Netherlands, 24 million healthy birds were killed in order to prevent the further spreading of the disease (i.e. pre-emptive culling) and for welfare reasons [34].

The BSE crisis has shown the impact of the media on major disease outbreaks. Personal stories of tragedy accentuated the human dimension and the consumer was portrayed as the innocent, vulnerable victim. Government, the farming industry and science were villains [62]. It can be suggested that media coverage with images of open-air pyres, burial grounds or landfill disposal of carcasses during mayor animal disease outbreaks significantly contributed to the public outcry for alternative management procedures.

Finally, the publics’ concerns about current disease management strategies not only include the disrespect of animal welfare and questioning the present way of conducting animal husbandry, but also the resistance against the culling of susceptible hobby animals and pets in protection and/or surveillance zones and the vulnerability of the environment such as groundwater pollution.

Vaccination

Vaccination strategies are faced with various implementation problems and are therefore not fully deployed. A vaccine’s usefulness is determined by the effectiveness for eliminating viruses of the specific serotype(s) that occur(s). Currently, vaccines are available for some serotypes of avian influenza, foot and mouth and bluetongue but not for BSE. However, as of yet there is no vaccine that protects against the bluetongue virus serotype that infects herds in Western EuropeFootnote 6.

Furthermore, preventive vaccination will sometimes not be used for economic reasons such as the costs of manufacturing, distributing and administering the vaccines and the fear that the vaccination policy might affect export markets and put off consumers. The latter refers to the possibility that vaccinated animals and their products contain the infectious agent and as such pose a risk when introduced into countries or zones that are free of the disease [55]. If preventive vaccination schemes are maintained they can imply a serious economic burden on the livestock sector, which already suffers from marginal profits. This type of reasoning led, for example, to the EU ban on preventive avian influenza and foot and mouth disease vaccination (EU Directives 92/40/EEC and 90/423/EEC).

The recovery of disease-free status varies according to which strategy is used. A country or zone where vaccination is not practiced can recover its disease-free status after 3 or 6 months. If vaccination is practiced, the recovery is delayed until 6 or 18 months depending on the application of stamping out.

Hence, partly due to economic reasons and partly due to efficacy reasons (e.g. immunization delays, herd immunity, vaccination effectiveness), EU policies for highly pathogenic avian influenza, foot and mouth disease, bluetongue and BSE still do not allow general preventive vaccination, but do allow for emergency vaccinations for highly pathogenic avian influenza and foot and mouth disease. The 2001 foot and mouth disease crisis in the UK changed the perceptions of stamping out and its main alternative, vaccination [65]:

Vaccination appeared the more ethical, civilized, and nationally beneficial policy; culling seemed a backward, immoral method, bringing shame on the nation, supported only by a selfish minority who sought to advance their own interests (in the livestock export trade) at the country’s expense.

Long Term Effects of Disease Outbreaks

Although public controversies around major epidemics can be particularly sharp, these responses are essentially short term effects. Le Gall [33] summarizes many—and more—of such effects, grouping them in direct effects, ripple effects, and spillover effects, remote effects, but also long term effects. The economic effects he identifies are mainly economic such as loss of consumer confidence, loss of access to markets and reduced productivity. One could add the opportunity cost of disease outbreaks (finances and energy that could be spent on better causes). There are long term influences that are ethically relevant, but not economically in nature, but there are few that are more than the aggregate of short term effects (i.e. the accumulation of short term effects of many outbreaks).

One could surmise that disease outbreaks could lead to an increased pressure on the conventional livestock industry with a subsequent move towards ‘alternative’ production systems.Footnote 7 However, in many cases these alternative systems are equally or more susceptible to those outbreaks. This is especially true with viruses such as avian influenza or foot and mouth disease that are transferred through the air (by birds, insects or independently). Furthermore, such systems are possible only in some regions of the world, and are not always able to deliver the same product at the same low cost, which would drive producers out of the market without an associated shift in demand. In short, it seems that if disease outbreaks are to influence production systems, most likely it will be a drive towards more intensive, i.e. more controllable systems. This negative ethical balance could further be aggravated if the disease becomes endemic or by the loss in biodiversity that might be associated with disappearing local breeds or euthanized zoo animals.

This paper focuses on the short term effects of disease outbreaks. The long term influences could be further discussed but it seems reasonable to believe that technologies relieving (some of) the short term problems will also be beneficial in the longer run. For instance, if nano-enabled diagnostics offer a technological solution for the differentiation between non-vaccinated infected animals and vaccinated healthy animals, this could shift the polarized debate between stamping out and vaccination in favor of the latter.

Relevance of Advanced Diagnostics for Animal Diseases

The variation in impact from Table 1 will contribute to the variable need or urgency of the development of nano-enabled diagnostics for further disease control, as summarized in Table 2. The importance for the protection of economics, human health and animal welfare will determine the importance for shortening the diagnosis time, i.e. the time needed to detect the disease in an animal. Diseases with a negative impact on all areas are to benefit more from shorter time between infection and detection. Foot and mouth disease and bluetongue have virtually no impact on human health. Hence, from this perspective, the need for earlier diagnosis is less important than investment in vector control and disease eradication. BSE, highly pathogenic avian influenza and bluetongue are lethal for respectively cattle, poultry and sheep, while foot and mouth disease is not for cattle, pigs and sheep and bluetongue is not for cattle. When human health is simultaneously combined with the perspective of economics, (direct and indirect costs of a potential outbreak) and with animal welfare (the avoidance of animal suffering), foot and mouth disease, BSE and highly pathogenic avian influenza have the greatest potential to benefit from advanced diagnostics.

Table 2 Importance of early detection of the infectious agent for further disease control
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Nano-enabled Diagnostics for Real-time Disease Monitoring

As can be concluded, both stamping out and vaccination collide with the expectations of cost-effective disease eradication or animal friendly disease management or both. Both strategies fail significantly due to the shortcomings of present diagnostics, often leaving authorities no other option than to pursue the radical stamping out strategy.

Research on implantable nano-enabled biosensors for pathogen and contaminant detection has not yet resulted in applications; recently however, biochips have shown promising progress towards recognition of multiple biological agents [67]. Biosensors and biochips (i.e. a set of individual biosensors) for implantable applications should exhibit minimal fouling and should be able to function under a wide range of biological conditions such as temperature, pH, humidity and enzymatic activity [15].

Until now, implantable biosensors for in vivo monitoring have been developed mainly to suit human needs (e.g. glucose monitoring; [64]). Few applications exist for veterinary ends, but in vitro detection of milk progesterone [66], Bovine Viral Diarrhoea [56] and mastitis [41] have been reported.

In the longer run, implantable biosensors can be integrated into on-farm sensing systems where the immunological activity of animals is constantly monitored through a network of sensors connected with a central information device. As soon as any disturbance is detected, appropriate measures can then be taken by stockholders, veterinarians or authorities. Both for intensive and extensive farming systems (especially dairy cattle), this online diagnostic system could be supplemented with existing tracking, identification and registration systems for such as electronic tag readers, injectable transponders and collars [48, 52].

On the conceptual level, the demands might be clear, but on the operational level many scientific and technological challenges are still unresolved. There are reasons for the slow technology transfer from research laboratories to the marketplace: cost, instability, sensitivity issues, quality assurance and instrumentation design [59]. In order to become a commercial and efficient early on-farm diagnostic tool, the sensor system should be easy-to-use in daily farm conditions, (relatively) inexpensive, and provide fast and accurate information. Furthermore, important technological challenges remain such as selectivity towards one or more analytes, the solution to possible interference with multiple analyses and/or with sensor signals, the organic or inorganic characteristics of the chip material, and calibration and resetting after detection. Functionality of electronics inside living organisms—an environment known to be unkind to non-biological components—demands additional stability requirements. Low power consumption and wireless communication are recommended as animals may bite or pick at the wires. Finally, data interpretation models have to be developed that can provide the stockholder or veterinarian with accurate and transparent information.

Ethical Evaluation of Nano-enabled Diagnostics with the ‘4-Principles’ Approach

Theory of the ‘4-Principles’ Approach

In this section we assume that implanted nano-enabled diagnostics are technologically feasible and that their integration in on-farm networks can be made operational. The implementation of advanced sensors will have ethical implications and will be shaped by societal deliberations. Reviews on the ethical impact of nanotechnology mainly elaborate on a list with ethical issues such as privacy, equity, control, security, environmental impact and human–machine interactions [30, 39, 40, 50]. Here we choose an alternative classification building on the experiences with decision making in biomedical ethics. This is based on a process of deliberative evaluation of the impacts of proposed actions with four prima facie principles: nonmaleficence, beneficence, justice and respect for autonomy [7, 37]. These principles are very general guides which need to be specified in each case and for each relevant actor.Footnote 8 The ‘4-principles approach or principlism’ of Beauchamp and Childress encloses the understanding of these principles as critical directives for ethical reflections. Essential in this approach are the identification and analysis of parameters that promote the respect for the principles and those that infringe them.

The Principles of Nonmaleficence and Beneficence

The nonmaleficence principle is an obligation not to inflict harm on others and is derived from the ancient maxim ‘Primum non nocere’ or ‘First, do no harm’. The principle of beneficence requires that we not only refrain from harming others but that we contribute to their welfare. Both principles are often proclaimed as the fundamental principles behind the Hippocratic Oath of health care professionals. The nonmaleficence principle can simply be met by inaction or by doing nothing (and hence, nothing bad), while the principle of beneficence requires an active action to promote the benefit of the other. Both principles reflect utilitarian concerns and could be integrated into the principle of wellbeing [38].

The Principle of Justice

Respect for justice is the moral demand for the fair access of services and goods to all treated people. It requires that equal cases are treated equally.

The Principle of Autonomy

Respect for autonomy is the obligation to value the autonomous choices and actions of other people and is one of the obligations under ‘respect for persons’ [31]. Respect for autonomy requires intentionality and agency and is the basis for the concept of informed consent and refusal [7]. In the case of a doctor treating a patient, autonomy can be specified into the right-to-know, the right-not-to-know and the duty-to-know. First, the right-to-know is a fundamental ethical and legal principle in human healthcare, granting the patient the right to be informed about a certain medical intervention or treatment. Secondly, recent advances in predictive genetic testing make an increasing number of people aware they are at risk of a serious disease without any real chance of reducing that risk, or of obtaining an effective treatment [1]. Hence, such people may have a desire not to be informed and this desire is called the right-not-to-know. Both the right-to-know and the right-not-to-know are principles explicitly recognized by recent ethical and legal instruments. Finally, the right-to-know and the right-not-to-know (as most rights) are not absolute. In some—often very delicate—cases such as parental decision-making about selective abortion following prenatal screening, the right-not-to-know can be turned into a duty-to-know. Doctors are then obliged to inform the parents about potentially harmful genetic disorders of their fetus. Hence, respect for autonomy is a very strong principle, but there can be situations where the overruling of this principle can be justified. Medical paternalism refers to the actions of a doctor without informed consent of the patient. According to Bassford [6], medical paternalism is justified only in a utilitarian framework and only if the patient is incompetent, has authorized the physician to act paternalistically, or is known so well by the physician that his preferences can somehow be deduced.

The ‘4 Principles’ Approach Applied to Nano-enabled Diagnostics in Livestock Production

Can these principles clarify some shortcomings of present disease strategies and/or advantages of nano-enabled diagnostics when they are applied to intensive livestock production? We propose that the discussion on the usefulness of nano-enabled diagnostic in livestock production can be facilitated using the four ethical principles. Each of the principles needs to be balanced against the others in order to determine the optimal course of actions. The following ethical discussion is but the tip of the iceberg; it can help to provoke a more extended debate on the ethics of livestock disease control. Research in the vast domain of nanotechnology is nascent and continuously being revised. Therefore, this preliminary assessment is open to a more extended follow-up awaiting further development of nano-enabled diagnostics in livestock production towards the commercialization stage.

The principles nonmaleficence, beneficence, autonomy and justice have not only be used in (bio)medical ethics but are increasingly being recognized in legislation. The normative discussion on morally good or bad actions is followed by regulation. Medical professionals are now obliged to treat their patients with best possible care and provide them with most accurate information available. In other words, ethical arguments have also become legal arguments. Will ethical arguments for or against the implementation of nano-enabled diagnostics also become legal arguments? While in the healthcare sector both activities and goals are anthropocentric or human-centered with a high degree of individuality, the livestock production sector is, at least in Europe, a mixture of human oriented goals and animal centeredFootnote 9 production processes with a strong emphasis on economics and societal interests. Medical health care deals with direct doctor–patient interactions; livestock production involves direct farmer–authority and farmer–animal interactions and indirect society–farmer and society–animal interactions. Despite the increased attention to animal welfare in some parts of the world, the value attributed to farm animals is still inferior to the value attributed to humans. Hence, ethical arguments in favor of more animal friendly disease management or more sustainable livestock production will not automatically be built into regulative frameworks. Practices that incorporate the trend towards a more animal friendly production are continuously confronted with economic feasibility. Furthermore, the medical health care and livestock production sectors are characterized by different relations between human actors. Doctors treat identifiable individual patients, while farmers produce for unknown consumers. This difference has important repercussions when something goes wrong. If a patient decides not to choose a medical implant for disease surveillance that the doctor advised, the negative economic consequences will be minimal for society in case the patient dies of a regular disease that could have been prevented by installing the implant. But if a livestock outbreak occurs, the negative economic consequences can be dramatic.

Principles of Nonmaleficence and Beneficence

Nano-enabled diagnostics will be designed to alert responsible actors and as such help to avoid negative effects of a disease outbreak. If there is no infectious agent, then the technology offers no direct advantages. It offers, at best, indirect benefits through the avoidance of disease management expenses that can then be used for other purposes. Therefore, this type of technology has more impact on the principle of nonmaleficence (avoiding harm to wellbeing), than on the principle of beneficence (promoting wellbeing). Hence, respect for the principle of wellbeing is mainly attributed by minimizing economic burdens and avoiding animal suffering (both part of the respect for the principle of nonmaleficence).

First, the economic component stems from the desire of livestock producers to earn a satisfactory income and of authorities to minimize disease management costs such as culling operation and compensation payments. If nano-enabled diagnostics are to be paid by individual farmers, daily reality urges that nano-enabled diagnostics also benefit producers directly. Nano-enabled diagnostics should at least not result in a lower income and subsidizing measures from governments should be proportional to the potential economic disadvantages of these sensors.

Secondly, animal suffering due to disease depends amongst others, on adequate diagnosis techniques and remediation. Better diagnosis does not automatically guarantee less animal suffering, but can contribute to better differentiation between infected and non-infected animals, hereby reducing the need for culling the latter. The lower number of animals that have to be culled allows disease eradication executers to perform the necessary culling more appropriate with respect to animal welfare. If the animals are not to be culled (e.g. bluetongue), earlier diagnostics can increase the available time for remediation.

Principle of Justice

Respect for justice refers to the fair distribution of the net profit made from the advanced diagnostics. This has to be considered between countries and regions, but also within regions and countries.

In most parts of the world there are no indications for a decreased consumption of animal processed products; in important areas consumption is increasing (rapidly). The high number of farm animals per production unit or per nation, is a clear indicator that there is a vast potential market for sensors in livestock production. Therefore, as soon as the technology becomes satisfactorily sound, prices will probably become affordable for producers and authorities.

Additional costs of new technology depend on the production cost, the potential number of animals, life span, compensation intervention and profits. First, production costs and number of animals are inversely related. In other words, nano-enabled biosensors for broilers will probably be cheaper than those for cattle as there are more broilers. Risk assessment models could refine the need whether each animal should be monitored or only a selection of animals that can act as ‘alarm triggers’. Secondly, the life span of animals equipped with these diagnostics is relevant to determine the economic cost. Dairy cattle for instance have a production cycle that is multiple times that of broilers. Other things being equal, investment in a unit of advanced diagnostics for a herd of cattle is less expensive than for a flock of broilers. Thirdly, additional costs of nano-enabled diagnostics may be reduced by compensation intervention from government subsidies or by higher profits from a higher consumer price. Finally, the continuous price decrease of commodities such as wheat and milk has recently stopped because of worldwide scarcity propelled by global warming resulting in failed harvests and the quest for alternative fuel sources on arable land. Depending on the nature of the commodity, some livestock sectors (e.g. dairy cattle) might benefit from increased margins while other sectors (e.g. pigs) may suffer from this scarcity. However, it is to be expected that this trend will make the nano-enabled diagnostics bearable even without compensation payments, at least for some sectors.

It remains to be established though, whether this analysis will hold for all producers. Large scale producers and producers in high-income countries (willing to subsidize nano-enabled diagnostics) are likely to be more able to invest in this technology than others. The result would inevitably be an uneven distribution of possible profits from the technology, but would not necessarily mean a weakened export position of the developing countries (as their export-oriented production is often controlled by very large companies).

It can, however, be expected that most applications will be developed with trade-restricting diseases in mind. These are not the solutions that will of most benefit to poor farmers, such as those in developing countries. Granted that the uptake of such technology will be difficult to these farmers without additional help, it seems that publicly funded research should focus on these other diseases if nano-enabled diagnostics are to be useful for poor farmers.

The latter also touches upon the distribution of the intellectual (and financial) property rights to this technology. It is clear that the large technology firms developing nano-enabled diagnostics will claim these property rights. Although their research effort needs to be rewarded, this will divert a large proportion of the net revenue towards these firms and it means that many ‘policy’ decisions will be made by them and not by state or OIE entities.

Principle of Autonomy

Finally, we believe that the principle ‘respect for autonomy’, as in bioethics, may play a decisive role in the decision-making process about the implementation of these technological applications. Respect for autonomy implies respecting the right to make autonomous decisions and this has to be considered within each stakeholder group. In other words, autonomy means something different for livestock producers, veterinary officials, citizens, consumers and animalsFootnote 10. We will specifically deal with the autonomy–paternalism dilemma, meaning the autonomy of the farmer and the paternalism of the disease management authorities.

Initially, it seems farmers have the right to use the nano-enabled diagnostics (right-to-know) in order to be informed about the health status of their herd, but they also have the right not to be (right-not-to-know). On the one hand, the farmers’ decision will be influenced by financial concerns such as the price of the sensor systems and the farmers’ financial situation. On the other hand, they might perceive those advanced diagnostics as an insult to their professional care-taking abilities, and, therefore, as an infringement of their autonomy. Farmers could then choose not to implement the technology or prefer a version that allows them to determine when the devices are sending information and when not. A function that allows the monitoring devices to be switched on and off could be a technological solution for the farmer’s dilemma between the right-to-know and the right-not-to-know. Then, preference would be given to the farmer’s autonomy.

A relevant question, though, is whether the farmer, as the custodian of the animals’ health and welfare, is not obliged to implement technologies that help protecting their health (duty-to-know)? If so, this would make price an ‘irrelevant’ factor, possibly resulting in conflicts with other rights, duties and economic realities.

Farmers, however, are not the only key players in disease management. Their interests or desires may conflict with those of others such as authorities. Authorities have a strong interest in a continuous stream of animal health data for adequate risk assessment. Therefore, as protectors of human and animal health (and the country’s economic position), they have the ethical right to know about diseases emerging within or close to their territory. It seems that in their position authorities can not decline this right-to-know (i.e. they do not possess the right-not-to-know), meaning they have the duty to know. This would mean authorities should take (legal) action to ensure that nano-enabled diagnostics are used as soon as the technology is sufficiently sound.

It is interesting to note that such a duty-to-know is already an internationally recognized principle in animal disease management, illustrated by the list of notifiable diseases such as BSE, foot and mouth disease, highly pathogenic avian influenza and bluetongue [43]. Thus, considering the decrease in price when large volumes are to be produced, and the need for additional disease information by the authorities it is to be expected that livestock producers will be (legally) denied the (ethical) right-not-to-know and will be obliged to implement this technology in daily livestock practices, imposing the duty-to-know. In any case, the ethically inspired (and by other arguments supported) national or supranational legally enforced duty-to-know would overrule the livestock producers’ initial right-not-to-know, which in practice means the balance in the autonomy–paternalism dilemma shifts towards the latter.

This exposes an interesting conflict between the practical implications of the rights and duties of individuals and authorities (societies). Awaiting further clarification of the duty-to-know argument in the case of farmers, some infringement of their autonomy seems likely. On the other hand, this needs not be neglected entirely. A weak paternalism can be achieved when the sensor network offers a technological possibility to discontinue the data flow. In that case, authorities could require farmers to install nano-enabled devices without enforcing a continuous data transmission. In times of increased risk, the government would then oblige farmers to activate the hitherto quiescent devices.

Finally, the principle ‘respect for autonomy’ may also differ in the stakeholder group of the broader public. Each individual has two frames that emerge in daily decision making: one of a citizen and one of a consumer [44]. As a citizen, one is more concerned with values of the common good, while a consumer wants to satisfy individual preferences. An individual’s behavior may show ambivalence as a result of discrepancies between perceptions and behavior [57]. The citizen frame emphasizes more non-monetary values such as animal welfare and more sustainable animal production, while the consumer frame is more concerned with monetary considerations. After all, each technology investment in disease control leading to an increase in product price, will be carefully weighted against human health risk probability and risk perception, trust in information sources and other consumer interests such as taste and visual quality characteristics. Milk, eggs and meat from animals equipped with miniaturized sensors could lead to consumer ambivalence from human health viewpoint. They might wonder whether these products could contain (parts of) these sensors. In an attempt to make a more robust conceptualization and prediction of consumers’ reaction, Pennings et al. [45] decoupled the consumer’s risk response behavior into risk attitude and risk perception. Whereas risk perception deals with the chance to be exposed to the content of the risk, risk attitude deals with the interpretation of content of the risk. Amongst other, such issues have to be taken into account if the expectations of citizens are to be consistent with consumer behavior.

Principles Approach and Sustainable Livestock Production

So far in this paper, the link between the approach based on moral principles and the concept of sustainability in livestock production has been rather implicit. This correlation is however not a trivial point as sustainability has been defined in numerous ways and, as Beauchamp and Childress acknowledge themselves, their principles need to be specified along the road. Through specification of the principles we have elaborated on economic, ecological and societal concerns that form the basis of the concept of sustainability. Other concepts such as sustainable development, sustainable agriculture and sustainable livestock production are derived from the general notion of sustainability.

The notion of sustainability encompasses a number of concerns and has varied throughout human history. Gamborg and Sandøe [25] describe that sustainability initially involved the regular harvesting or extraction of a natural resources for human purposes. Since the 1980s, the notion not only includes biodiversity preservation, but also distributive concerns in relation with future generations (Brundtland report; [63]) and between the developed and developing countries (Rio Declaration; [47]).

Sustainable livestock production is frequently defined as ecologically sound, economically viable and socially just [3]. It is not only a practical approach but also a question of attitude. However, the actual content of the ecological, economic and societal pillars have to be specified according to the specific agricultural system and is often subject to overlapping discourses and dynamic interpretations. The judgment of sustainable livestock production can never be a final judgment, as the multidimensional nature of the concept incorporates different appreciations of people towards ecological, economic and societal dimensions. Disease management supplemented by means of diagnostic devices can, at best, result in a more sustainable livestock production.

If and Then? Critical Evaluation of Nano-Enabled Diagnostics in Livestock Production

New technological (r)evolutions are not easy to predict. It is not the scope of this article to predict exactly when these nano-enabled diagnostics will be daily practice in livestock production. It may be in 10, 20, 50 years or even later. As the previous sections show, there are several concerns that currently impede the implementation of advanced diagnostics in livestock production and these concerns range from insufficient scientific knowledge, technological constraints, and economic and socio-ethical uncertainties. However, we expect a gradual evolution from technological unfeasible, economically unbearable and societally wanted to technological feasible, economically bearable and societally accepted.

Real-time monitoring of health status of animals is not technologically feasible at the moment. But it is fair to assume that livestock production will benefit from research on implantable biosensors from nanobiotechnology in human medical sciences. At present, monitoring, storing and processing of vital parameters in and on the human body, and the possibilities of remote supervising by a doctor are investigated intensively worldwide. Once the technology is available for human applications, the knowledge might be transferred to livestock production. The actual implementation into the system will ultimately be determined by the economic and socio-ethical deliberations. This trade-off will result in the acceptance or disapproval of this technological revolution and can be influenced but will not be dominated by scientific and technological realizations on the longer term.

Conclusions

At present, research in the fields of nanoscience and nanotechnology is booming. This might give the impression that nano-enabled diagnostics for livestock production are business-as-usual applications under the nano-umbrella and that socio-ethical deliberations about autonomy and paternalism only happen in the periphery of the technological evolution. However, nanotechnology is still in an early phase of development and gives us the opportunity to outline the rules that (should) apply to complex issues, such as newly emerging technologies, in order to stage an appropriate interaction between scientists, technologists, farmers, authorities and society. This interaction should minimally result in technological devices and a regulative framework that support responsible behavior and minimize unwanted negative consequences.

Stamping out practices with a disproportionate number of culled healthy animals are inconsistent with the increased attention to sustainable livestock production. In this article, the possibilities of nano-enabled diagnostics—as a new way to deal with epidemic animal diseases—were explored. Such advanced diagnostics can be a valuable, ethical solution if they manage to offer technological answers to the issues of safety and autonomy–paternalism. The safety issue includes a differentiation between non-vaccinated infected animals and vaccinated healthy animals in order to shift balance between stamping out and vaccination in favor of the latter. The autonomy–paternalism issue refers to the dilemma of the individual farmer’s preference to stay autonomous, while authorities may find it justifiable to override this preference in the case of a serious disease outbreak or threat. Hence, the technology should allow to be switched on/off by farmers. However, there should be maneuvering space for society to protect itself from harm by bestowing upon farmers a weak paternalism in the form of a duty-to-know.

It is not suggested nano-enabled diagnostics will free future livestock disease eradication strategies of culling of infected animals. However, by reducing the time until detection of a disease, they can significantly improve the time for appropriate control and eradication and as such greatly reduce the number of culled animals. Miniaturized diagnostics with satisfying operational performance and technological specifications appear to address some shortcomings of present diagnostics and hence could contribute to a better balance between stamping out, vaccination and prophylactic measures.