State of the art in benefit–risk analysis: Food microbiology

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This page (including the files available for download at the bottom of this page) contains a draft version of a manuscript, whose final version is published and is available in the Food and Chemical Toxicology 50 (2012) 33–39. If referring to this text in scientific or other official papers, please refer to the published final version as: S.H. Magnússon, H. Gunnlaugsdóttir, H. van Loveren, F. Holm, N. Kalogeras, O. Leino, J.M. Luteijn, G. Odekerken, M.V. Pohjola, M.J. Tijhuis, J.T. Tuomisto, Ø. Ueland, B.C. White, H. Verhagen: State of the art in benefit–risk analysis: Food microbiology. Food and Chemical Toxicology 50 (2012) 33–39 doi:10.1016/j.fct.2011.06.005 .

Title

Editing State of the art in benefit–risk analysis: Food microbiology

Authors and contact information

S.H. Magnússon, Corresponding author
(Matís, Icelandic Food and Biotech R&D, Iceland, Tel.: +354 422 5000; fax: +354 422 5001,

E-mail: sveinnh@matis.is.)

N. Kalogeras
(Maastricht University, School of Business and Economics, The Netherlands)
G. Odekerken-Schröder
(Maastricht University, School of Business and Economics, The Netherlands)
H. Gunnlaugsdόttir
(Matís, Icelandic Food and Biotech R&D, Iceland)
F. Holm
(FoodGroup Denmark & Nordic NutriScience, Denmark)
O. Leino
(National Institute for Health and Welfare, Finland)
J.M. Luteijn
(University of Ulster, School of Nursing, United Kindom)
M.V. Pohjola
(National Institute for Health and Welfare, Finland)
M.J. Tijhuis
(Maastricht University, School of Business and Economics, The Netherlands)
(National Institute for Public Health and the Environment, The Netherlands)
J.T. Tuomisto
(National Institute for Health and Welfare, Finland)
Ø. Ueland
(Nofima, Norway)
B.C. White
(University of Ulster, Department of Pharmacy & Pharmaceutical Sciences, School of Biomedical Sciences, Northen Ireland, United Kindom)
H. Verhagen
(National Institute for Public Health and the Environment, The Netherlands)
(Maastricht University, NUTRIM School for Nutrition, Toxicology and Metabolism, The Netherlands)
(University of Ulster, Northern Ireland Centre for Food and Health, Northern Ireland, United Kindom)

Article info

Article history: Available online 12 June 2011

Abstract

Over the past years benefit–risk analysis (BRA) in relation to foods and food ingredients has gained much attention; in Europe and worldwide. BRA relating to food microbiology is however a relatively new field of research. Microbiological risk assessment is well defined but assessment of microbial benefits and the weighing of benefits and risk has not been systematically addressed. In this paper the state of the art in benefit–risk analysis in food microbiology is presented, with a brief overview of microbiological food safety practices.

The quality and safety of foods is commonly best preserved by delaying the growth of spoilage bacteria and contamination by bacterial pathogens. However, microorganisms in food can be both harmful and beneficial. Many microorganisms are integral to various food production processes e.g. the production of beer, wine and various dairy products. Moreover, the use of some microorganisms in the production of fermented foods are often claimed to have beneficial effects on food nutrition and consumer health. Furthermore, food safety interventions leading to reduced public exposure to foodborne pathogens can be regarded as benefits. The BRA approach integrates an independent assessment of both risks and benefits and weighs the two using a common currency.

Recently, a number of initiatives have been launched in the field of food and nutrition to address the formulation of the benefit–risk assessment approach. BRA has recently been advocated by EFSA for the public health management of food and food ingredients; as beneficial and adverse chemicals can often be found within the same foods and even the same ingredients. These recent developments in the scoping of BRA could be very relevant for food microbiological issues. BRA could become a valuable methodology to support evaluations and decision making regarding microbiological food safety and public health, supplementing other presently available policy making and administrative tools for microbiological food safety management.

Abbreviations

ALOP, Appropriate Level of Protection; BENERIS, Benefit–risk assessment for food: an iterative value-of-information approach – project; BRA, Benefit–risk analysis; BRAFO, Benefit–risk analysis of foods – project; CAC, codex alimetarius commission; DALY, disability-adjusted life year; EFSA, European Food Safety Authority; EU, European Union; FAO, Food and Agriculture Organization; FOSIE, Food Safety in Europe: Risk Assessment of Chemicals in the Food and Diet – Project; FSO, Food Safety Objective; GMP, good manufacturing practices; HACCP, Hazard Analysis Critical Control Point; HIC, health impact criteria; ILSI RF, International Life Science Institute Research Foundation; IPRA, Integrated Probabilistic Risk Assessment; LYL, Life-Years Lost; MID, minimum infectious dose; MRA, microbiological risk assessment; PHIA, Probabilistic Health Impact Assessment; PO, Performance Objective; QALY, Quality-adjusted Life Year; RIVM, [Dutch] National Institute for Public Health and the Environment; WHO, World Health Organization; QMRA, quantitative microbiological risk assessment; QALIBRA, quality of life-integrated benefit and risk analysis, Web-based tool for assessing food safety and health benefits – project.

Keywords

Risk assessment, Microbiological risk assessment, Benefit–risk assessment, Food microbiology,

Introduction

Microbiological food safety management is aimed at minimizing the risk of food borne illness and the application of microbiological risk assessment for the management of food safety is well established. Risks from microbiological hazards (pathogenic bacteria, viruses and parasites) are of serious concern to food safety and human health. International and domestic food safety policies and regulations are based on the assumption that our food should be safe and if there are reasonable grounds for suspecting there is a problem, actions should be taken to limit the risk (EU, 2000, 2004). Risk analysis is the traditional approach used by food safety managers and policy makers for controlling and assessing food safety (FAO/WHO, 1995). Risk assessment is the science based component of risk analysis, along with risk management and risk communication (FAO/WHO, 1995, 1997).

Over the last few years the application of benefit–risk assessment in relation to food and food ingredients has gained considerable attention. Where food or foodstuffs have the potential of exerting both beneficial and adverse effects on public health, the importance for risk managers to be able to weigh the health risks against the health benefits has been advocated (EFSA, 2006, 2010). Benefit–risk assessment integrates the results of two separate activities; risk assessment and benefit assessment and can be defined as an approach that weighs the probability and severity of harm as a consequence of exposure against the probability and magnitude of benefit (FAO/WHO, 2008).

No food carries zero risk for microbiological hazards but the risk varies considerably depending on different types of hazards and food matrices as well as the susceptibility of individual consumers. Benefit assessment and benefit–risk assessment relating to microbiology have not been well defined as microbial contaminants in food generally only have neutral or adverse effects on human health, and rarely are directly beneficial for human health. Probiotic bacteria are however commonly considered to confer direct health benefits to humans, although the majority of such health claims have been rejected by EFSA (http://www.efsa.europa.eu/ en/ndatopics/topic/nutrition.htm). Furthermore, many microorganisms e.g. various yeast and lactic acid bacteria are used in food processing e.g. wine, beer, cheese and yogurt and although they are not directly beneficial to human health they are integral parts of a variety of food production processes (Steinkraus, 1996; Doyle and Meng, 2006). More importantly, benefit–risk analyses may also include the weighing of the benefit of reduced risk of adverse health effects due to pathogenic microorganisms. In this paper we discuss the potential value of using benefit– risk analysis (BRA) in the management of microbiological food safety. The paper presents an overview of existing approaches to microbiological food safety and risk analysis as well as on benefit– risk analysis (BRA) in food microbiology.

Microbiological food safety and risk analysis

Microbiological food safety

Microbiological food safety is centered on the production of safer foods and mainly ensured by preventive approaches. Its primary goals are to minimize the risks of foodborne pathogens and their toxins, reduce the incidence of human disease as well as facilitating domestic and international trade (EU, 2004). Microbiological risk is managed by governmental standards and regulations on distinct levels of foodborne hazards that may not be exceeded (ICMSF, 2005). The current level of tolerable or acceptable risk the community is willing to accept is a political decision by risk managers and commonly termed the ‘‘Appropriate Level of Protection’’ (ALOP) (Gorris, 2005). Although standards on foodborne pathogens are relatively few, the accepted levels of some of the most common pathogenic contaminants and indicator organisms in food products are dictated by the European Union (EU) general food law (EC: 2073/2005) as well as national legislation.

The management of microbial food safety has evolved from mainly relying on product testing to process control approaches such as the implementation of good manufacturing practices (GMP) and the Hazard Analysis Critical Control Point (HACCP) principle (EFSA, 2007). More recently, risk-based management concepts have been introduced. Including the application of risk based managerial tools that dictate the limits of acceptable microbiological hazards in food e.g. Food Safety Objective (FSO) and Performance Objectives (PO). These new terms have been implemented in an effort to relate and communicate ALOP’s and public health goals set bygovernments to the food industryand allow for food safety targets to be translated into assessable parameters (ICMSF, 2005).

Risk analysis

Over the past decade food risk regulators have adopted risk analysis as an approach for assessing, communicating and managing risks in relation to food safety. Risk analysis is a structured approach consisting of three components; risk assessment, risk management and risk communication. Risk assessment is the analytical component of risk analysis (Smith, 2002; Renwick et al., 2003), more specifically it is a process where the likelihood and magnitude of harm posed by specific hazards is evaluated (FAO/ WHO, 1995). Risk management has been located in the domain of politics and legislation. It includes the process of weighing policy alternatives based on the results of the risk assessment. Risk communication is the interactive exchange of information and opinions concerning risk assessment and risk management and has traditionally been located in the domain of the social science (Fischer et al., 2005). The risk analysis approach is accepted as a common operation framework for the control of microbiological food safety by the FAO/WHO (Food and Agricultural Organization and World Health Organization) and is a fundamental approach underlying food safety standards (FAO/WHO, 1995, 1997; Lammerding and Fazil, 2000).

Microbiological risk assessment

Historically food risk assessment has its roots in concerns for toxic chemicals in food and has been adopted by food microbiology as a tool for the management of the risks caused by foodborne pathogens. Microbiological risk assessment (MRA) can be defined as the scientific evaluation of known or potentially adverse health effects resulting from human exposure to pathogenic microorganism (Miliotis et al., 2008). MRA is commonly divided into four separate components: hazard identification, exposure assessment, hazard characterization (dose–response assessment) and risk characterization (Buchanan et al., 2000; Lammerding and Fazil, 2000). A framework of guidelines and principles for conducting MRA has been provided by the Codex Alimentarius Commission (CAC) (CAC, 1999).

There are two common approaches for microbiological risk assessment, qualitative and quantitative assessments. Qualitative assessments are descriptive evaluations, based on categorical information analysis that describe the risk as the likelihood of illness (e.g. high vs. low) (Lammerding and Fazil, 2000; Schroeder et al., 2007). Qualitative assessments are commonly performed when there is lack of scientific data, time or resources for quantitative modelling, or prior to quantitative assessments in order to evaluate the significance of the risk (Lammerding and Fazil, 2000; Giaccone and Ferri, 2005). Quantitative microbiological risk assessments (QMRA) require a substantial amount of numerical data for estimating risk in a statistical manner by mathematical modelling. QMRA presents the predicted risk as distributions or probability, often using the number of disease incidence per annum, lives lost, or as of recently, by integrated health metrics e.g. the DALY (Giaccone and Ferri, 2005).

Microbiological food safety differs fundamentally from chemical food safety, yet the risk assessment framework for microorganisms and chemicals is the same (Ashbolt, 2004). Unlike chemical contaminants, microbes can enter food at any point of the food chain or during processing, while chemical residues and additives typically enter the food chain at more or less predictable points. Also, microbes are capable of multiplying and interacting with the food during storage and as conditions change (Havelaar et al., 2009). Furthermore, dose responses to foodborne pathogens are highly variable, depending on various factors e.g. the virulence characteristics of different pathogens or strains, number of ingested cells, the general susceptibility of individual consumers as well as the attributes of the food matrix. These interactions all influence the dose–response relations (Buchanan et al., 2000).

Dose–response and thresholds

The major difficulties experienced when performing quantitative microbiological risk assessments their substantial data requirement. Determination of food safety levels would ideally be determined through detailed knowledge regarding the dose response relations for the pathogen in concern (Julien et al., 2009). However, pathogen exposure levels are commonly low and assessing the shape of the dose response curve can be challenging, therefore a full quantitative assessment of human pathogens is not possible many cases (Buchanan et al., 2000, 2009; Havelaar et al., 2000). Traditionally, a threshold level of pathogen has been assumed to be needed to lead to infection, commonly referred to as the ‘‘minimum infectious dose’’ (MID) (FAO/WHO, 2003). The MID entails that pathogens have a particular dose level below which the organism is not expected to cause disease. The threshold methods and the use of MID have been criticised after a series of outbreaks associated with consumption of low levels of pathogenic bacteria (Buchanan et al., 2009). Recently, linear non-threshold mathematical models have been incorporated to describe the dose–response curve. These models assume that there is no minimal infectious dose but that a single cell has a very small but finite probability of causing illness (Buchanan et al., 2000; FAO/WHO, 2003). In the light of the challenges posed by dose–response assessments, new options for addressing low dose effects have emerged e.g. the Key Events Dose–Response Framework (KEDRF), an analytical framework developed by an International Life Science Institute Research Foundation (ILSI RF) working group (Julien et al., 2009). The KEDRF is based on the notion that an improved understanding of the underlying biology of infection is the optimal strategy for refining best dose–response assessments and predictive models. KEDRF involves an examination of all the major biological steps following an intake of adverse biological agents and is centred on the identification of ‘‘Key Events’’ leading to infection (Buchanan et al., 2009; Julien et al., 2009). The approach can be applied to a wide variety of bioactive agents including foodborne microbiological pathogens (Buchanan et al., 2009; Taylor et al., 2009) and gives insight into the connection between the biological processes underlying infection and the outcomes observed at individual and population levels (Julien et al., 2009).

Benefit–risk assessment

Table 1 Examples of food microbiological scenarios warranting BRA.

Scenarios Description Risks Benefits
Disinfectants Benefits from the use of disinfectants to kill pathogens in food processing vs. harmful residues of chemical byproducts in the food Harmful chemical residues Reduced exposure to pathogens (risk mitigation)
Preservatives The risks of salt addition for food preservation vs. risk of cardiovascular disease Cardiovascular disease, promoting selection of resistant pathogens, unrevealed long term health effects Reduced risk of infection, prolonged shelf life, increased product quality (risk mitigation)
Preservatives The benefits of nitrite addition to tackle Clostridium botulinum growth in comparison to the risks of nitrosamine formation Stomach cancer, promoting selection of resistant pathogens, unrevealed long term health effects Reduced risk of infection, prolonged shelf life, increased product quality (risk mitigation)
Probiotics The risks and benefits of probiotics and the biosafety of starter cultures Potential health risks for parts of the population Claimed to improve digestion and induce ‘‘good’’ microbes
Minimally processed food Benefits of minimally processed foods vs. the risks of microbiological contaminants Potentially higher exposure to pathogens Potentially higher nutritional value
Globalization of food supply Benefits from the globalization of the food supply and changes in food processing and farming practices vs. new challenges from microbiological hazards Transportation of pathogenic bacteria from resistant human population to susceptible populations. Rapid distribution of pathogenic bacteria Higher food supply security, diverse food, nutritional diversity


Table 2 Summary of case studies relating to microbiology that formulated a benefit–risk question.

Field of study Methods Summary References
Disinfectants – biocides

Ozonation of drinking water

Two independent quantitative risk assessments compared using DALY Quantitative assessment on the risks and benefits of drinking water ozonation. Benefits of reduced exposure to C. parvum weighed against the risk of ozonation by-products (bromate). Health benefits of reduced pathogen exposure found to be 10-fold higher than risks of bromate. Uncertainties in assessing the DALY noted Havelaar et al. (2000)
Pesticides

Fungicides vs. mycotoxins

Two independent IPRA risk assessments (Integrated Probabilistic Risk Assessments) and comparison of IMoE distributions (individual margins of exposure) Comparison of the health risks posed by fungicides to the benefits of reduced exposure to mycotoxins via food. None of the toxic compounds found to have adverse effects on public health Muri et al. (2009)
Antibiotics

Ban on the use of growth promoting antibiotics in poultry farming

Quantitative probabilistic risk assessments Risk of Campylobacter infections due to consumption of poultry weighed against the benefits of ban on antibiotic use (enrofloxacin or macrolides) against bacterial illness in poultry. Benefits from ban found to be unlikely to exceed human health risks posed by ban Cox and Popken (2004)
Antibiotics

Ban on the use of growth promoting antibiotics in food animals

Quantitative risk assessments using RTTT framework (Rapid Risk Rating Technique). Comparison expressed in QALY Quantitative assessment on the benefits of reduced incidence of antibiotic resistant Enterococcus faecium (VREF) weighed against the risks of increased Campylobacter exposure to consumers due to ban on virginiamycin (VM) in food animals. Increased incidence of

Campylobacter infections due to termination of VM use expected to outweigh benefits of reduced incidence of VREF infections

Cox (2005)
Food safety

Benefits of healthy dietvs. food safety

Quantitative risk–risk comparison using DALY Quantitative assessment on the benefits of healthy diet and risks concerning food safety. Health gains by improvements of diet far exceed gains attained by improving food safety Kreijl et al. (2006)


The benefit–risk assessment approach

The BRA approach has been advocated for the public health management of food and food ingredients, as beneficial and adverse potentials can often be found in the same foods and even in the same ingredient (EFSA, 2010). Benefit–risk assessment approach integrates the results of two separate activities, risk assessment and benefit assessment. Comparing the probability of adverse health effects as a consequence of exposure against the probability of benefit, if both are known to be possible (EFSA, 2010).

While definitions and procedures for risk assessment have been well established, both through governmental bodies, (e.g. CAC) and in the scientific literature, guidelines for performing benefit assessment and benefit–risk assessment have not been well defined. Several EU funded projects, including: BENERIS (www.beneris.eu), QALIBRA (www.qalibra.eu) and BRAFO (www.brafo.org) have been working in the field of food and nutrition on the development of a benefit–risk methodology that enables assessment of the overall impact of particular dietary choices on health. Recently a benefit–risk assessment guidelines document has been finalized by the European Food Safety Authority (EFSA) scientific committee (EFSA, 2010).

Risks and benefits in food microbiology

Balancing microbiological and chemical risks has been a public health issue of concern for decades, particularly in relation to the use of pesticides and disinfectants (Keane, 1972; Bellar et al., 1974), while the benefits and risks of human vaccination and use of antibiotics in food-animals have also been a topic of debate (Howson and Fineberg, 1992; Casewell et al., 2003). The use of benefit– risk analysis for the management of microbial hazards, by assessing the balance of risks and benefits in a systematic manner using composite metrics, is however a new field of research and to date a very limited number of studies have been performed.

Microbiological food safety generally does not require an assessment of benefits as the consequences of microbial contaminants are usually only adverse; depending mainly on different types of hazards and foods as well as the susceptibility of individual consumers and consumer groups to infection or intoxication (Buchanan et al., 2000). However, interventions leading to the reduction of microbiological risk can be regarded as a positive effect and a public health benefit. Various methods are commonly used for controlling microbiological contamination in foods and drinking water as well as during food processing. Preservatives (e.g. salting, sodium-nitrate and sugar addition) are used for limiting microbial growth and increasing product shelf life. Disinfectants (e.g. active chlorine addition, ozonation) are used to tackle microbiological contaminants in the food processing environment and drinking water. Fungicides are used for control of mycotoxin producing fungi, etc. Most if not all applications used for controlling microbiological health risks create an alternative risk to public health, often a chemical risk; warranting the evaluation and balancing of both risks and benefits (reduced risk) for public health management.

To the best of our knowledge, all published studies related to BRA in food microbiology are not direct evaluations of risks and benefits, but rather intervention assessments or risk comparisons studies, independent risk assessment of two diverse hazards (Havelaar et al., 2000; Cox and Popken, 2004; Kreijl et al., 2006; FAO/WHO, 2008; Muri et al., 2009) (Table 2). BRA studies directly weighing the impact of risks and benefits were not found in our literature survey, this highlights the novelty of the BRA approach as a concept for microbiological food safety management.

Weighing risks and benefits

An integral part of the benefit–risk assessment approach is the comparison and weighing of health risks and benefits. This approach requires the application of a standard metric for describing adverse and beneficial health effects in the same unit of measure. Comparing across different health endpoints requires the use of an integrated measure of risk. The DALY and QALY are currently the most commonly used metric unit for evaluation of public health (Murray, 1994; Gold et al., 2002). Applying severity weights to different disease, allows for the DALY to be used for a direct comparison of disease with different endpoints and public health impacts and can allow for the direct comparison of adverse and beneficial effects on human health (Havelaar et al., 2000). Currently however, there are no agreed metrics for positive health effects and well being (EFSA, 2010). For more details on the benefit– risk assessment approach in food and nutrition refer to Tijhuis et al. (in press).

The DALY concept is mainly applicable for ranking adverse health effects that can be translated to human disease as life years lost (LYL). In the case of many toxicological hazards this is however difficult or impossible (van Klaveren and Boon, 2009). In such cases a semi-quantitative measure would be preferable to the DALY. For a more detailed discussion on the DALY and common metrics in the benefit–risk assessment approach refer to Tijhuis et al. in press. The health impact prioritising system for evaluating health impacts has been introduced as an alternative to the use of DALYs and QALYs (Bos et al., 2009). The health impact prioritisation system was developed within the EU funded SAFE-FOODS project (Bos et al., 2009). The health impact is divided into four categories, separated by three levels of health impact, so called health impact criteria (HIC). Different health effects in HICs at the same level are assumed to have an equally adverse health impact. Integrating the HIC to the Integrated Probabilistic Risk Assessment (IRPA) model, also developed within the SAFE-FOODS project, for the comparison of health risks between adverse chemicals (van der Voet and Slob, 2007) results in a Probabilistic Health Impact Assessment (PHIA) model that can be used for semi-quantitative assessments of chemical risks with different toxicologically adverse effects (van der Voet and Slob, 2007).

The PHIA model has been used by Muri et al. (2009) to compare and weigh health risks associated with fungicides and mycotoxins (see also Table 2). The methodology has not been applied for measuring beneficial effects, but could be used for comparing risk factors and reduced pathogen risk and be advantageous for application in food microbiological BRA.

BRA scenarios in food microbiology

Various scenarios concerning microbiological hazards that warrant consideration of risk benefit assessments have been identified and discussed (EFSA, 2006, 2010; FAO/WHO, 2008). These include cases of chemicals applied to prevent microbial growth, as well as cases where enhanced nutritional value due to improved processing needed balancing against possibly greater survival of pathogenic bacteria (EFSA, 2006, 2010; FAO/WHO, 2008). Table 1 presents a few microbiological scenarios that might warrant benefit– risk assessment.

The majority of identified scenarios in Table 1 involve the comparison of the health benefits/risk of specific food items or production processes and the risk of microbial infections – or the benefit of reduced bacterial load. Probiotics is the only case where the microorganisms themselves are directly linked with the beneficial effect on human health.

Risks and benefits of probiotic bacteria

While microbiological contaminants in food in the majority of cases have adverse effects on human health, many microorganisms are integral to various food production processes e.g. the production of beer, wine and various dairy products and some microorganisms in food are considered directly beneficial to human health. These microorganisms are termed probiotic, which by FAO/WHO definition are, ‘‘living microorganisms that confer health benefits to a host when administered in adequate amounts’’ (FAO/ WHO, 2002). Probiotic bacteria predominantly belong to the genera Lactobacillus and Bifidobacteria (Isolauri et al., 1991; Kekkonen et al., 2008), along with some strains of Enterococcus and Saccharomyces (Donohue, 2006). Bacteria with a potentially probiotic activity are currently considered and evaluated under EU regulation 1924/2006 on health claims on food (Verhagen et al., 2010). Numerous studies have indicated beneficial health effects of probiotics (Rayes et al., 2002; Bousvaros et al., 2005; Kekkonen et al., 2008). In addition, they are generally regarded as safe because of their long history of use as well as being part of the normal commensal microflora (Ouwehand and Salminen, 2003; Donohue, 2006). They are rarely associated with disease, and are thought to have low pathogenicity (Bernardeau et al., 2008). Yet, some studies have shown that a small portion of the population may be at risk of adverse effects following probiotic administration (Reid, 2006; Besselink et al., 2008; Sanders et al., 2010). Immunicompromised patients have for example been found to be susceptible to opportunistic Lactobacillus spp. infections (Husni et al., 1997; Schlegel et al., 1998), although it has not been determined if these Lactobacillus strains are consistent with those found in food. As mechanisms of interaction of so-called probiotics with the host and colonizing microbes are largely unknown, the interpretation of such effects is difficult, and the relevance therefore not yet well understood. Strains produced in the food industry are being isolated and propagated, and substrains may emerge. The genetic stability of the bacterial strain over time, deleterious metabolic activities and the potential for pathogenicity and toxicity need to be assessed, depending on the genus and species of the microbe being used. Some applications of the microbes pertain to stimulation of the immune system. However, over-stimulation of the immune system may lead to adverse consequences, and immunological effects must be considered in terms of potential adversity, especially in certain vulnerable populations, including infants with underdeveloped immune function (Sanders et al., 2010). An area that is a cause for concern is that the microbes meant to be probiotic are known to harbour antibiotic resistant genes and have been suggested to be capable of transferring antibiotic resistance to pathogens that can be transmitted to humans through the food chain via the commensal flora (Courvalin, 2006). For these reasons the use of BRA approach for evaluating probiotic safety has been advocated, although the approach on how to carry out this assessment has not been precisely formulated (Donohue, 2006).

Case studies

The methodology of balancing risks and/or balancing risks and benefits in microbiological perspective has to date most notably been used for evaluating risk factors related to applications for reducing microbiological exposure to humans. Most if not all applications used for controlling microbiological health risks create an alternative risk to public health, often a chemical risk; warranting the evaluation and balancing of both risks and benefits (reduced risk) for public health management. Case studies related to food microbiological topics that formulated a benefit–risk question could not be found in the literature, and all related studies could be regarded as risk–risk assessments (Table 2). However, some groups have suggested that an intervention that leads to reduction in risk may be regarded as a positive health effect or benefit. In such cases, the reduction in microbiological risk achieved by the chemical or alternative intervention might be regarded as a positive health effect and thus is weighed as a benefit in a benefit– risk assessment. In fact, risk–risk and benefitrisk assessment are analogous approaches and could be performed in a similar manner. In the following section we therefore discuss in more detail a case study performed by Havelaar et al. (2000) on the balancing of microbial and chemical risk. This is in essence a risk–risk assessment nevertheless it warrants a brief discussion as it sheds a light on the approaches used to carry out a quantitative microbiological BRA.

Balancing the risks and benefits of drinking water disinfection

Havelaar et al. (2000) were among the first to demonstrate a systematic approach for comparing microbiological and chemical risks in a quantitative manner using composite metrics to compare risk and benefits of microbiological and chemical hazards with differing disease endpoints. They estimated the beneficial effects of reducing the load of the protozoic parasite Cryptosporidium parvum in Dutch drinking water vs. the health risks of carcinogenic bromate (an ozonation by-product) formation following drinking water ozonation. They used probabilistic risk modelling to quantify the chemical and microbiological risks, respectively, expressing them in DALYs. The results from their models indicated that the health benefits of reducing C. parvum outweigh the health loss due to bromate formation by a factor of 10. Their study demonstrated that the DALY could be used effectively to weigh health risks and benefits of disease with differing endpoints and public health impacts and to assess the net change in public health following regulatory actions. Nevertheless, they conclude that gaps in the available data for performing quantitative analysis and assessing DALYs are large, and can be expected to result in a large degree of uncertainty, hampering the precision of quantitative assessments (see discussion in Section 2.4).

Microbiological benefit–risk management

As previously emphasised, the primary and traditional goal of microbiological food safety is to minimize exposure of foodborne pathogens to humans and protect public health. Furthermore, the primary goal of risk management is to control risks through selection and implementation of appropriate protective measures (FAO/ WHO, 1997). Accepted levels of microbiological contaminants in food are focused on consumer protection and dictated by national and international standards and legislation.

The application of benefit–risk management relating to microbiological contaminants is based on the principle of protecting human health, same as that of general risk management. However, the BRA approach broadens the view of microbiological food safety and risk management. Instead of focusing solely on minimizing the exposure to foodborne pathogens and protecting the public from foodborne infections, BRA proposes that the managerial decisions that overall leads to the best outcome for the general public health or the health of specific subgroups should be administered. BRA advocates that administrative decisions should be based on the weighed assessments of both risks and benefits using integral units of measure. For each scenario an assessment of both the risks and the benefits to public health should be identified. Subsequently, the administrative decision that promotes the most overall benefit to public health should be promoted, based on the weighed comparison of individual assessments. Focusing solely on guaranteeing food safety and thereby not allowing food benefits to occur is equally well a risk management decision as that of proposing for instance the lowering or increasing of a current safety level for a particular pathogen or for certain foods, if by doing so added health benefits can be gained for the general public or population subgroups.

Conclusion and recommendation

Benefit–risk analysis concerning microbiology is an important issue for food safety management. However, BRA is a relatively new research field in microbiology that needs to be explored further; risk assessment is well defined but assessment of benefits or weighing of benefits and risks has not been systematically addressed. BRA has advanced further in the field of food and nutrition. We propose that those practices could be adopted by food microbiology, as has previously been done regarding microbiological risk assessment, and food microbiology actively participates in the discussion and scoping of the benefit–risk analysis approach. Similarities of microbiological BRA and risk–risk assessment are great, as many microbiological scenarios that warrant BRA relate to the reduction of pathogen exposure; the benefits of reduced risk. However, we note that quantitative studies related to food microbiology have demonstrated that lack of data may in many cases hamper the direct quantitative comparison of risks and benefits. The BRA methodology of balancing benefits and risks could become a valuable tool for decision making regarding microbiological food safety and public health issues; and supplement other presently available policy making and administrative tools (e.g. risk assessments and cost-benefit assessments) regarding public health and microbiological food safety management.

Conflict of Interest

The authors declare that there are no conflicts of interest.

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