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Zoonoses and Public Health

ORIGINAL ARTICLE

Toxicants Exposures as Novel Zoonoses: Reflections on Sustainable Development, Food Safety and Veterinary Public Health C. Frazzoli1,2 and A. Mantovani1,2 1

Department of Veterinary Public Health and Food Safety, Food and Veterinary Toxicology Unit and WHO/FAO Collaborating Centre for Veterinary Public Health, Istituto Superiore di Sanita`, Rome, Italy 2 Noodles ONLUS, Nutrition & Food Safety and Wholesomeness, via Luigi Mancinelli, Rome, Italy

Impacts • Veterinary public health actions towards novel zoonoses associated with toxic exposures of food producing animals. • Safety of foods of animal origin as a component of sustainable development, including Hazard Analysis and Critical Control Points systems for toxicological risk management. • Long-term, transgenerational impact of novel zoonoses in industrialized and developing countries. Keywords: Communicable diseases; Early warning; endocrine disrupters; HACCP; sustainable food safety; risk analysis Correspondence: C. Frazzoli. Department of Veterinary Public Health and Food Safety, Food and Veterinary Toxicology Unit and WHO/FAO Collaborating Centre for Veterinary Public Health, Istituto Superiore di Sanita`, viale Regina Elena 299, 00161 Rome, Italy. Tel.: +39 (0)6 4990 2528/2815; Fax: +39 (0)6 4990 2658; E-mail: chiara.frazzoli@iss.it Received for publication January 13, 2009 doi: 10.1111/j.1863-2378.2009.01309.x

Summary The modern concept of zoonosis considers any detriment to the health and/or quality of human life resulting from relationships with (other) vertebrate or edible or toxic invertebrate animals. Whereas exposure to toxicants through foods of animal origin (a.o.) is a well-established issue, hereby we discuss it as novel zoonoses, from the standpoints of health implications as well as similarities and differences with classical zoonoses caused by biological agents. Novel toxicant-related zoonoses are linked with new issues in food safety, such as the environment-feed-food chain. In fact, the potential effect of the combined and repeated exposure to dietary toxicants is generally long-term and not readily discernible. Endocrine disrupting chemicals in staple foods of a.o. are discussed as a telling example of a food safety issue summing up critical points covered by the definition of sustainable development, also implicating health risks for generations to come. We suggest some critical points to implement the veterinary public health action in sustainable food safety, such as enhancement of Hazard Analysis and Critical Control Points systems for toxicological risk management.

From Food Inspection to Food Hygiene and Food Safety The control of foods of animal origin (a.o.) deeply changed during the last century along with the perception of human health risks associated with live animals and their products. Foodborne diseases are defined by the WHO as diseases of an infectious or toxic nature caused by, or thought to be caused by, the consumption of food or water. With the semi-intensive rearing and the small food-processing industry, the traditional food inspection practice was enhanced with food hygiene tests at the slaughtere136

house and/or at laboratory. At that time, diseases transmittable by farm animals or their products to humans represented a major group in foodborne zoonoses. The development of intensive rearing and great processing industry brought about the introduction of new and multiple risk factors, with the use of chemical, biological and pharmacological aids in animal productions and the related international alarms. As a consequence, the control of foods of a.o. has a changing place within the food safety framework; control programmes need updating based on new production chains, globalization as well as new farm animal exposure patterns and disease scenarios. ª 2010 Blackwell Verlag GmbH • Zoonoses Public Health. 57 (2010) e136–e142


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Human exposure to chemicals through foods of a.o. is a recognized topic in food safety, which is related to many problems concerning, e.g. regulatory management and residue analysis of chemicals used in animal production (Macrı` and Mantovani, 1995; Mantovani et al., 2006). In the last decade, attention has gradually shifted towards the assessment of potential health implications of chemical intake through foods of a.o.; for instance, some concern exists about the characterization of endocrinerelated effects of residues (Mantovani and Macrı`, 2002). Therefore, toxicants in foods of a.o. have nowadays to be considered as a veterinary public health issue. Potential effects of chemical contaminants and residues are generally long-term and not readily discernible, thus entraining new aspects of foodborne diseases. The awareness of such long-term effects elicited an extension of the zoonoses concept, that Adriano Mantovani (2000) defined as ‘Any detriment to the health and/or quality of human life deriving from relationships with (other) vertebrate or edible or toxic invertebrate animals’. The Alma Ata Declaration stated that prevention and control of zoonoses is a most important function of public health (WHO, 1978). The field of zoonoses, classically related to infectious agents and space-dimension (diseases spreading) perspective, is extended to include toxicant-related not-epidemic hazards associated with environment-to-foodborne exposures; such risk factors spread through the time-dimension perspective also by implicating health risks for next generations. Indeed, the widespread, combined and repeated exposure to dietary toxicants of the general population may change the extent of the population to be protected: this may occur when chemicals may affect the health burden of such vulnerable subgroups as developing organisms, therefore leaving a detrimental heritage to future generations. Sustainability and Food Safety Chemical exposure through foods of a.o. is a novel zoonosis with potential transgenerational implications; this in itself relates to the sustainability concept, all the more considering the Brundtland Report, that defines as sustainable the development that ‘meets the needs of the present without compromising the ability of future generations to meet their own needs’ (Brundtland, 1987). The key point of sustainable development is to avoid irreversible damages to natural capital in the long-term (including chronic diseases and impaired progeny health) in turn for short-term benefits; its pillars lay in environmental and socio-economical determinants of health. According to an evidence-based assessment, the burden of endocrine, metabolic and reproductive diseases is related to individual lifestyles as well as to ‘living environment’ factors, hence ª 2010 Blackwell Verlag GmbH • Zoonoses Public Health. 57 (2010) e136–e142

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to sustainability (Olden and White, 2005). Thus, prevention requires knowledge of environmental health factors, especially those affecting potentially more vulnerable groups, e.g. foetuses and children particularly in socioeconomically disadvantaged communities. Food is one living environment factor that is shared by the whole general population, while safety of food is strictly connected with environmental quality, lifestyles and socio-economic status. Sustainability of food production in terms of, e.g., energy and natural resource consumption is an emerging topic (Gussow, 2006). Moreover, the new concept of ‘sustainable food safety’ has been recently introduced as ‘the complex of actions intended to minimize also adverse health impact on future generation associated to today’s safety and nutritional quality of food’ (Frazzoli et al., 2009, 2010). The White Book of the European Commission (from farm to fork) (Commission of the European Communities (CEC), 1999) and the establishment, in 2003, of the European Food Safety Authority (EFSA) represented innovative steps towards the contemporary food safety approach aimed at a ‘whole-chain’ system integrating animal disease prophylaxis plans and control strategies for contaminants and residues in feeds, live animals and their products. In this context, endocrine disrupting chemicals (EDCs) are a telling example of a food safety issue summing up critical points: (i) potential for long-term effects, (ii) multiple exposure throughout whole diet and bioaccumulation, and (iii) concern for vulnerable lifecycle phases, from the unborn through to the pubertal child (Mantovani, 2006). Noticeably, the ‘Weybridge definition’ states that an EDC can cause adverse health effects through hormone-related mechanism(s) in an intact organism, or its progeny (European Commission, DG Environment, Endocrine Disrupters Website, http://ec.europa.eu/environment/endocrine/ index_en.htm). The potential of EDCs for multiple exposure through different steps of the food production chain as well as for multiple developmental targets is exemplified by their heterogeneity. Indeed, EDCs include compounds used in plant and/or animal production (fungicides, antiparasytic drugs and herbicides such as benzimidazoles, dicarboximides, triazoles, triazines) as well as persistent organic pollutants that are able to bioaccumulate (dioxins, polychlorinated biphenyls – PCBs, DDT and related pesticides) and chemicals still widely present in industrial and/ or consumer products, that may also bioaccumulate in some instances (brominated flame retardants, phthalates, bisphenol A, etc.). Anabolics used in cattle production, and currently forbidden in the EU, are also EDCs. Moreover, concern is increasing towards hormone-related effects of heavy metals chemical forms/species (especially arsenic and cadmium) as well as of plant-derived compounds that can be present in foods as natural e137


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components (e.g. soy phyto-oestrogens and goitrogens) or undesirable substances (e.g. the mycotoxin zeralenone). Endocrine disrupting chemicals may contaminate food chains according to several scenarios: some are forbidden in industrialized countries but still persist in the environment (e.g. DDT), others are allowed and monitored in food control programmes even though current maximum residue limits may need an update (e.g. antifungal compounds such as azoles), yet others are widespread but control over exposure though foods of a.o. is still limited (e.g. brominated compounds). Toxicological studies on EDCs provide a wealth of long-term effects on the next generation arising during the intrauterine life. To obtain evidence in human studies is more difficult; however, examples are the vaginal adenocarcinomas following maternal intake of diethylstilboestrol, and the EDC-associated ‘testicular dysgenesis syndrome’ which increases the risk of infertility and seminomas in adults (Sharpe, 2003). Indeed, transgenerational effects of dietary factors, including toxicants, may cover a much broader range than currently thought: limited but not negligible examples of transgenerational impact (grandparents–parents–progeny) include the transfer of (i) permanent epigenetic alterations relevant to metabolic disorders, (ii) metabolic status as well as (iii) cultural approach to food and dietary habits. Risk assessment and management of EDCs in foods of a.o. is linked with new issues in food safety, such as the environment-feed-food chain. EDCs may accumulate in agricultural lands and be available for uptake by grazing livestock. Long-term toxicity may disrupt farm animal production; most importantly, farm animals may carry over to consumers significant amount of residues without any overt sign of toxicity (Mantovani et al., 2008). The consumer, especially the most vulnerable groups, needs to be protected from this inadvertent, often poorly controlled and potentially long-lasting intake. Accordingly, the concept of zoonoses is currently extending to all human health effects related to noxious factors from animals and animal products; therefore, awareness should increase that zoonoses do include foodborne health disorders linked to chemical exposures (Macrı` et al., 2006). Environmental and Socio-Economical Determinants of Toxicant Related Not-Epidemic Risks In the different world areas, the population is exposed to complex mixtures of EDCs throughout life according to varying scenarios. One effect of food contamination by EDCs is the reduced availability of foods, whose supply should be protected because of their nutritional benefits as well as their marketability. For instance, nutritional characteristics and affordable cost of rice and fish make them e138

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staple food items in many countries. However, these foodstuffs may accumulate environmental EDCs, e.g. arsenic and dioxins/PCBs respectively; implementing effective food control programmes will protect the population from long-term health risk, but will also lead to a lower availability of staple foods. Thus, development of a toxicological risk-to-nutritional benefit approach is required (EFSA, 2007). Risk-to-benefit approaches should take into account the specific scenarios and needs of each Country and no fixed rules can be given, but only a general guidance. The specific ground for performing risk-to-benefit analysis should be explained in a clear and transparent way; benefit assessment should be performed in a parallel way as risk assessment. Most importantly, in certain situation of developing countries, the risk-to-benefit analysis can be critical: stricter food safety requirements may reduce the availability of nutrients with a significantly greater impact than in more affluent situations. On the other hand, there may be a tendency towards overlooking long-term health risks potentially extended to the next generations as those associated with EDCs exposures. For instance, factors altering the maternal endocrine homeostasis and placenta do alter foetal growth and body composition, with longterm consequences on the functional programming of metabolism and body systems. Attention to foodborne chemical risks is not a ‘luxury’ reserved to industrialized countries. The increasing obesity incidence is warning that health risk patterns are changing worldwide. In particular, in countries living the turning point in social-economical development the food system could be particularly at risk. In fact, emergencies associated with the control and management of health and environmental adverse effects of new and/or insufficiently controlled chemicals are likely introduced through rapid and unplanned urbanization, industrialization, intensive rearing, increasing demand for proteins of a.o. and sophisticated food. Further, technological dumping of harmful materials and improper waste disposal make the general population and generations to come exposed through the food chains to a multitude of harmful chemicals (such as metals, brominated flame retardants and NDL-PCBs), including highly toxic mixtures of EDCs from e-waste (dioxin-like compounds as PAHs, PCDDs, PCDFs and DL-PCBs) (Frazzoli et al., 2009, 2010). Thus, emerging countries may be more vulnerable to long-term, transgenerational risks. Critical Points to Implement the Veterinary Public Health Action in Sustainable Food Safety The sustainable food safety framework requires that, when food scarcity is overcome, primary prevention of longterm risks becomes crucial (Frazzoli et al., 2009, 2010). ª 2010 Blackwell Verlag GmbH • Zoonoses Public Health. 57 (2010) e136–e142


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The concept of ‘sustainability’ should clearly include the needs of future generations in term of unimpaired potential for growth, development and health: for instance, the risk of chemicals, such as agrochemicals, veterinary drugs or feed additives, used/produced to solve problems in the short-term but that can persist into the environment must be carefully assessed; transnational collaborative control programmes have been already issued for persistent organic pollutants; such programmes might be extended to other potential global topics as well. Similarly, activities producing in the long run a significant output of toxic waste should be kept under control in a timely way: indeed, all practices linked to possible adverse impacts in the long-term may also result in a wider gap between developed and developing countries. Several aspects characterizing the precautionary principle are intrinsic to the sustainable development (Petrini, 2007), such as the duties of early detection and intervention, of weighing both the magnitude and the probability of unacceptable harms, and of caring for future generations. Veterinary public health can have a great role in the implementation of sustainable food safety, and several specific fields for action can be envisaged. A few examples may be mentioned, as given below. i) Encourage collection and analysis of study cases of toxicant exposures relevant to veterinary public health. Such comprehensive collection should include natural toxins, environmental contaminants as well as chemicals used in farm animal productions and agricultural practices. Accordingly, examples may include: the feed-tofood transfer of aflatoxins and presence of aflatoxins M1 in milk and dairy products (EFSA, 2004); methylmercury in different seafood and exposure of vulnerable consumer groups (Maycock and Benford, 2007); the potential impact of pesticides on the honeybees industry and use of honey as bioindicator (Balayiannis and Balayiannis, 2008); the risk assessment of the environment-to-food carry over of mixtures of lipophylic pollutants (TurrioBaldassarri et al., 2009); the use of metabolism data to guarantee the safety of veterinary drug use for consumers (Anado´n et al., 2008). It will be important to include these and other study cases within the basic training in veterinary public health. An important support to achieve this goal can be provided by scientific associations already active in the field; a longstanding internationally recognized example is The American Board of Veterinary Toxicology (ABVT, http://www.abvt.org/public/index. html). ii) Use the widely established Hazard Analysis and Critical Control Points (HACCP) system based on a systematic analysis of each step of food production to identify critical hazards and control points for the whole ª 2010 Blackwell Verlag GmbH • Zoonoses Public Health. 57 (2010) e136–e142

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food chain quality management and the food safety assurance. To date, the HACCP system is systematically applied throughout the food-chains for food microbiology and its potential of enhancing food safety and preventing many cases of foodborne diseases is recognized worldwide (Food and Agriculture Organization of the United Nations, FAO, 1998). The new concept of sustainable food safety and toxicant-related zoonoses call for HACCP strategies covering also hazards other than those for acute foodborne diseases. A strategy combining HACCP and risk assessment has to be developed, covering the identification/control and, where possible, the removal of the hazards caused by toxicants along the relevant steps of the food chains. For instance, origin, type and silage conditions of feed ingredients are CCPs for controlling presence of aflatoxins M1 in milk; as pointed out also by the EFSA, this is not an issue confined to developing countries (EFSA, 2004). iii) Develop innovative, user-friendly and cost-effective technologies to provide a significant support for monitoring strategies and risk assessment/management and for detecting new markers to be adopted in routine control of food-derived hazards (Frazzoli et al., 2008). These novel tools, such as (bio)sensor batteries, might allow the early identification and correction of potential hazards in the production chain of foods of a.o.: such tools might link food safety and food security. iv) Promote research on wildlife; several bioindicators and biomarkers related to chemical pollutions have already been identified. For instance, in aquatic environments bioindicators at population level range from imposex in molluscs to demographic patterns in birds (Oehlmann et al., 2007; Bustnes et al., 2008); biomarkers include vitellogenin and other less-established biochemical changes in fish as well as immune alterations with increased susceptibility to infections in marine mammals (Hutchinson et al., 2006; Fossi et al., 2007; Sørmo et al., 2009). Notwithstanding research advances, field use of animal sentinels for environmental surveillance has been somewhat overlooked till now. However, the increasing implementation of molecular markers in ecotoxicological studies makes it timely their transfer into environmental control in the field. Identification of pollutants is not enough; sensitive, early markers of effective dose are needed to monitor long-term effects of contaminants and especially mixtures in real-life, field situations, possibly at lowest levels of the trophic chain; in its turn, the timely identification of biologically active levels of environmental contamination is needed to build a timely alert system (see, e.g. the PREVIENI project, http://www.iss.it/prvn/ ?lang=2). Veterinarians dealing with wildlife populations may, thus, make a great deal of work to protect environmental health and food production chain. e139


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v) Following the approach of the environment-feedfood chain, adopt strategies for the prevention and, where possible, for the recovery of contaminated animal feeds with ingredients like oil seed-, cotton seed- and coconut cakes, peanuts and corn grits, from natural contaminants as mycotoxins (Bhat and Vasanthi, 2003; Kabak et al., 2006; Schatzmayr et al., 2006). vi) Finally, among animal food production chains, improve aquaculture as recognized major and growing provider of food as well of nutritional benefits for all population segments, including foetuses and children. However, aquaculture is also highly exposed to persistent pollutants, mainly EDCs, which in their turn may specifically impact on developmental life stages. The exploitation of new ingredients in the formulation of aquaculture feeds is needed (CEC, 2002). For instance, the AQUAMAX project (http://www.aquamaxip.eu/) of the 6th EC Framework Programme targets the replacement of the fish meals and oils currently used in fish feeds with sustainable, alternative feed ingredients without affecting the growth performance, or the health and welfare of the fish, but increasing its health benefits and its acceptability to the consumer. Conclusions As the broadened concept of zoonoses encompasses health implications of the human-animal relationships, toxicants exposures through foods of a.o. may be, indeed, considered as a major issue within the zoonoses topic. A veterinary public health approach should therefore take into account differences, as well as similarities, between infectious and toxicant-related foodborne zoonoses. With regards to the differences, surveillance plans for toxicantrelated zoonoses often point at quantifying the agent level in foods, without paying attention to relevant health effects on both animals and humans. The detected levels are generally compared with ‘safe’ (acceptable/tolerable) limits, which are, in most cases, established on the basis of toxicological experiments using a precautionary approach; as a consequence, levels of potential toxicants may be detected that are of no concern for consumer safety, as they are below the ‘safe’ limits. Moreover, toxic hazards may arise from the (incorrect) intended use of chemicals such as antibiotics, antiparasytic drugs or feed additives, whereas any ‘intended’ use of infectious zoonotic agents is most unlikely. One obvious difference stems from specific concepts and terms, such as incubation and reservoir for infectious zoonoses and residues and bioaccumulation for toxicant-related zoonoses. Most importantly, in general, toxicant-related zoonoses are not readily discernable neither on animal nor human populations; no acute foodborne illness is to be expected, e140

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whereas they may reveal their health effects in the longtime. Thus, toxicant-related zoonoses are much less amenable to effective diagnosis and treatment. Such differences should not lead, however, to overlook similarities that stem from a common veterinary public health ground. In both cases, the noxious agent is transmittable from the animal to the consumer; therefore the physiology and metabolism of the living animal organism are critical components of human exposure. The onset and extent of the risk is strongly associated with characteristics of the productive chain (feed, living environment of farm animals, social and cultural features); therefore, both infectious and toxicant-related zoonoses are prone to be managed within the same prevention and control framework. The basic conceptual framework of risk assessment is the same, where effects have to be identified and their relationship with dose established, exposure/ carry over scenarios have to be outlined as well as worst cases have to be characterized; indeed, toxicant-related zoonoses may be considered as communicable due both to carry over from food producing animals to human, and the mother-child transmission of several major pollutants. Finally, critical agent/animal (or animal product) pairs are identifiable: examples are Campylobacter/poultry, Campylobacter/milk and perfluorinated organic compounds/fish. Thus, in both cases such pairs are major determinants for the exposure management and hence, for risk prevention and control. In the field of veterinary public health and food safety, the application of the sustainability concept means protecting the population, including the next generations, from long-term risks. This unavoidably means some rebuilding of priority settings and resource allocation by addressing knowledge and resources towards innovative rapid alert approaches and updated control strategies for the environment-feed-food chains and animal health. Obviously, to include sustainability among key issues of food safety policies, the dissemination of science-based and sound awareness about sustainable food safety should also involve regulators and policy makers in developing/ emerging countries. Veterinary public health can identify several specific issues for research and/or action to play a cutting-edge role in sustainable food safety in both industrialized and developing countries. Acknowledgements The manuscript has been elaborated in the frame of PREVIENI (http://www.iss.it/prvn/?lang=2) and 6th FP IP AQUAMAX (http://www.aquamaxip.eu). Authors acknowledge the support by the Noodles.ONLUS (http://www. noodlesonlus.org). ª 2010 Blackwell Verlag GmbH • Zoonoses Public Health. 57 (2010) e136–e142


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