Seguridad Aliment Aria 1

Download as docx, pdf, or txt
Download as docx, pdf, or txt
You are on page 1of 17

REVIEW

published: 21 February 2020 doi:


10.3389/fsufs.2020.00016

Food Security, Safety, and


Sustainability—Getting the
Trade-Offs Right
Ivar Vågsholm 1*, Naser Shah Arzoomand 2 and Sofia Boqvist 1
1
Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, Uppsala,
Sweden, 2 Division of Food Control, National Food Agency, Uppsala, Sweden

The United Nations sustainable development goals include eradication of hunger. To feed 10
billion persons 2050, we need to get the trade-offs right between sustainability, food security,
food safety, and make better use of food already produced. The hierarchy of strategies for
reducing food losses and waste are in descending order source reduction, reusing or
reprocessing surplus foods, recycle food as feed for animals, recover the energy as biofuels,
nutrients as compost, or raw materials for industry, while as last resorts one may consider
recovering the energy by incineration or dumping as garbage in landfills. This paper will
explore the trade-offs inherent when aiming at triple goals of sustainability, food security, and
safety looking at these strategies for reducing food losses and waste and resource footprints.
Intensification of food production and circular food systems could be parts of these solutions
to future food security. In this regard could our future trade-offs be informed by the
experiences from the use of antimicrobials to intensify food production and from the
Edited by:
Janne Mikael Lundén,
outbreak of bovine spongiform encephalopathy (BSE) in terms of circular food production?
University of Helsinki, Finland There is no trade-off between intensification of food production aided by antimicrobials and the
Reviewed by: public health risks from antimicrobial resistance due to the zoo-technical use of antimicrobials.
Séamus Fanning, A sustainable future requires control of antimicrobial resistance. If one avoids that cycles of
University College Dublin, Ireland
Riikka Keto-Timonen, nutrients become cycles of pathogens and/or hazards, circular food production systems will a
University of Helsinki, Finland major contribution to the future sustainable food security. Source reduction i.e., limiting food
*Correspondence: losses and waste appears to the strategy most promising for achieving sustainability. By using
Ivar Vågsholm
[email protected]
artificial intelligence and intelligent packaging major progress is possible, with the added benefit
of better control of food fraud. A changed diet—eating more plant-based foods and not eating
Specialty section: animal protein produced by edible feedstuffs, and source reduction of the food lost or wasted
This article was submitted to
Agro-Food Safety,
should enable us to feed at least an additional billion persons. Solutions to sustainability and food
a section of the journal security should integrate food safety considerations from the start.
Frontiers in Sustainable Food Systems
Keywords: source reduction, circular food systems, food loss and waste, antimicrobial resistance, BSE
Received: 25 July 2019
Accepted: 04 February 2020
Published: 21 February 2020
INTRODUCTION
Citation:
Vågsholm I, Arzoomand NS and
Food safety and security are two complementing elements of our sustainable future. This paper
Boqvist S (2020) Food Security,
will argue that in the long run the aims of food safety and security must be aligned to achieve
Safety, and Sustainability—Getting the
Trade-Offs Right. sustainability, and the trade-offs between these three goals must be managed carefully and
Front. Sustain. Food Syst. 4:16. based on evidence. Hence, we need novel solutions for our future food security and
doi: 10.3389/fsufs.2020.00016 sustainability

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

without compromising food safety to achieve the United (Johnstone and Mazo, 2011). Hence, food
Nations sustainable development goals (SDG) including
eradication of hunger and poverty, clean water, sustainable land
use, responsible production and consumption, mitigating
climate change, and sustainable life on land and water. Several
approaches are possible for achieving sustainability and food
security, such as limiting food losses and waste, eating more
plant based foods or recycling foodstuffs. The trade-offs
between food safety and security are fraught with challenges,
e.g., when constructing circular food production systems where
nutrients are recycled, one could also get a cycle accumulating
pathogens.
The tools and strategies used to achieve food security must
align with food safety, and public health as well as
sustainability. Food chains are complex and not transparent,
hence we believe a One Health approach is needed to assess
trade-offs and achieving sustainability (Boqvist et al., 2018). In
addition, the control of food frauds are an emerging issue
requiring attention. Getting the trade-offs right, between the
security, safety, and sustainability of food production, will
require careful balancing between multiple concerns and
challenges. In this balancing exercise could previous failures
inform us—for example antimicrobials used for intensifying
animal production, and the failed circular food and feed system
based on meat and bone meal (MBM) that caused the mad
cow disease epidemic (Bovine Spongiform Encephalopathy,
BSE)?
This paper explores and discusses some of the trade-
offs between sustainability, food security and food safety.
The discussion will follow the outline and food recovery
hierarchy suggested by the US Environmental Protection
Agency (Figure 1), but focus on the most promising options at
the top of the hierarchy.

SUSTAINABLE FOOD SECURITY A


POLITICAL IMPERATIVE AND CHALLENGE
Sustainable food security will require: (a) availability of food
or sufficient food production, (b) access to food and ability to
purchase food, (c) sufficiency in terms of nutrition including
energy, proteins and micronutrients as well as safety, and (d)
the stability and foreseeability of these conditions (Helland and
Sörbö, 2014).
Threats to food security include limited supplies of
nutritious and safe foods or when the consumers’ food purchasing
powers is limited (Bazerghi et al., 2016). Food insecurity affects
low-income groups most with increased risks of hunger and
malnutrition The International Monetary Fund (Arezki and
Brückner, 2011) found in low-income countries a correlation
between rising food prices and social unrest. Social unrest and
wars result in consequent food insecurity and famines.
However, the question whether initial food insecurity are a
driver for and triggers unrest is complicated (Helland and
Sörbö, 2014). It is raising food prices together with failing
political institutions, social safety nets, demographic pressures
and presence of other grievances, that is associated with
social unrest. The Arab spring 2011 is one example of where
spiking food prices was one of the drivers for social unrest

Frontiers in Sustainable Food Systems | www.frontiersin.org 2 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

insecurity is a serious threat to public health, social sustainability,


and political stability This challenge is magnified as the world
population is foreseen to increase to nearly 10 billion 2050
(United Nations, 2019). This 10 billion people will eat a diet
richer in animal protein (Sundström et al., 2014). The main
reason is that 3 billion people will shift toward a diet richer in
meat, fish, poultry, and dairy foods. Hence, feeding 10 billion
people in a sustainable way will probably require disruptive
changes of the food supply chains during the next 20 years
(AT Kearney, 2019). Moreover, the reduction of food losses
and food 1waste
FIGURE is part
| The food of the
recovery solution.
hierarchy. From upper most desirable source reduction to the least desirable at the bottom—landfill.
Another challenge is the diversion of edible crops (e.g.,
corn, sugar cane) to biofuel production. These diverted crops to
biofuel could have provided food for 400 million people
(Helland and Sörbö, 2014). Moreover, these diversions makes
the prices of biofuel crops more correlated to oil prices than
to supply and demand of food. Another concern is the
increasing speculation in food prices, as hedge funds become
greater players in the markets for food commodities as wheat,
oilseeds, and corn. Increasing the variability of food prices
poses a risk to food security for low-income groups.
A rapid urbanization has resulted in that more than half
of the global population is living in cities, which is another
challenge to food security. As urban consumers are
dependent on being able to purchase foods, the food security
of low- income urban populations are susceptible to increases
in food prices or unpredictable variations of food prices, in
particular of staple foods in countries with incomplete
socioeconomic safety nets. Moreover, relying on imports
may not be the solution

Frontiers in Sustainable Food Systems | www.frontiersin.org 3 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

as some countries impose export restrictions of foods in times food and thereby threatening sustainability. The links between
of limited food supplies. Hence, solutions to long-term food sustainability, food insecurity, and food waste are important.
security becomes national aims that might explain the drives More than one third of the food produced is lost or wasted
for developing novel sources of food and animal feedstuffs along the production chain (Lipinski et al., 2013). These lost
and resilient food chains. Several reports have addressed and wasted foodstuffs amount to 24% of the energy content of
these challenges. the food produced, illustrating the huge potential of improved
The EAT Lancet Commission on healthy diets from food security. By eliminating global food waste and loss, one
sustainable food production (Willett et al., 2019) suggested could feed more than one billion additional persons. Less food
several dietary changes to enable feeding a world with 10 lost or wasted would lead to more efficient land use and better
billion people in a resilient way. In brief, the recommendation water resource management with positive impacts on climate
was to double the consumption of fruits, vegetables, nuts, and change, livelihoods, and sustainability. In conclusion reducing
legumes and to halve the consumption of red meat and sugar. food losses and waste is a well-reasoned political objective. For
A diet rich in plant-based foods and with fewer animal source example, the European Parliament (European Parliament,
foods confers both health and environmental benefits. Another 2017) adopted a resolution to reduce food waste in the
example is the AT Kearney (AT Kearney, 2019) report on the European Union by 30 and 50% in 2025 and 2030, respectively.
disruptions from novel meat alternatives on the global food The two approaches foreseen in its resolution were to make food
production systems. The report suggested that meat will be donations easier and make “best before” and “use by” labels less
replaced by vegan or vegetarian meat replacements, insect based confusing. The world’s fisheries and fish farming can illustrate
meat replacements, and/or cultured meat i.e., meat produced some of these food loss challenges. Fisheries and fish farming
in bioreactors. Animal proteins such as milk, eggs and products contribute to nearly 20% of human protein consumption
thereof will be easier to replace, as the structures and (Moffitt and Cajas-Cano, 2014). However, the food losses are
biochemistry are simpler. The report suggests that in the future considerable, as 20 to 30% of the catch is lost at sea (FAO,
animal proteins and energy i.e., meat, milk and eggs, should be 2012), while another 10–15% of the catch is diverted as feed
produced using feed sources not suitable for human for fish farming resulting in protein and energy losses.
consumption e.g., pastures, grass, hay, or by-products. Of the total harvest of cereals and vegetables, nearly half (46%)
Food safety and food security are by necessity complementing is used as feed to animals while only around one third is used
aims for achieving freedom from hunger. One tenet is that unsafe to feed people. The feed conversion from plant to animal-
food do not solve food security problems. However, measures based food means that most of the edible energy and proteins
to ensure safety and quality of food can sometimes reduce the are lost in the conversion. For example, 10 kilograms of edible
amount of food available, and thereby amplify food scarcities. grains feed to cattle, produces only 1 kg of edible beef. The
For example, consumers interpret best before dates as food possibilities for increasing conventional meat, milk and egg
being poisonous thereafter dates thus increasing food waste production based on cereals are constrained by lack of
and threatening food security. Massive and not targeted food additional arable land and water, as well as difficulties in
recalls are other examples of food waste due to safety intensifying agriculture and animal production (AT Kearney,
concerns. 2019). The restrictions posed by land use, biodiversity, fresh
Environmental sustainability is part to a varying degree water use, greenhouse gas emissions as well as nitrogen and
of all the 17 sustainable development goals (SDG—https:// phosphorus cycling determine the sustainability and resilience
sustainabledevelopment.un.org). One key message though is that of food systems. In this regard, it appears that doubling of
environmental sustainability is a part of social and economic animal food production will require expansion of cereal and
sustainability as well as food security and safety. The pursuit of vegetable production beyond sustainable levels (AT Kearney,
one goal could be to the detriment of other goals. Hence, we need 2019).
to balance these goals and manage the trade-offs.
Causes of Food Losses and Waste
Food losses might be the result of pre-harvest failures. For
FOOD LOSSES AND WASTE VS. FOOD example, in a US study of pre-harvest losses of vegetables,
SECURITY more than half of the vegetable crops were not harvested
(Johnson et al., 2018) indicating a huge potential for increased
FAO (FAO, 2011) defined food loss as lost supplies along the food food production. The edible and wholesome vegetables
chain between the producer and the market while food waste (cucumbers, zucchini, bell pepper, cabbage, eggplant, yellow
is discarding safe and nutritious foods. Around one third of the squash) available for recovery amounted to 8,840 kg per hectare.
food produced is lost. The foodstuffs lost and wasted represent Food losses occurs also at harvest and post-harvest due to
around 28% of the world agricultural area and 8% of global problems in processing, handling, packing, transportation, and
greenhouse emissions. Moreover, reducing food waste and losses retail. Some of the underlying causes of food loss include the
will represent a major business opportunity valued at more inadequacies of infrastructure, cold chains, skewed incentives
than 400 billion USD (Unilever Reducing food loss and waste, or lack of legal frameworks—waiting for customs clearance.
2019) according to Unilever, a leading global food company. Tomatoes crushed during transport because of improper
Food loss and waste represent also the lost labor, capital, packaging is one example of food loss. Food waste, on the
water, energy, land and other resources that went into other hand, refers to the discarding of food that is safe and
producing the nutritious
Frontiers in Sustainable Food Systems | www.frontiersin.org 4 February 2020 | Volume 4 | Article 16
Vågsholm et Food Security, Safety, Sustainability Trade-Offs

for human consumption for example binning tomato cans if the sustainability. Should food security be thought of as an insurance
labels on the can is incomplete or the labels was peeled off. question—how much to pay in premium to ensure that we do
The reasons for food loss and waste include: not suffer famine, get right nutrition, and avoid food borne
• Failure and consequent spoilage in the agricultural process, illnesses in the future? The term nega-watt triggered a lot new
harvest, storage, processing, packaging, and marketing; thinking in the energy field (Lovins, 1990). The most resource
• Abnormal reduction of quality such as bruising of packages, friendly watt was the one not wasted or lost, hence
fruits or vegetables; investments in saving energy was just as efficient as
• Quality flaws—e.g., fresh produce that deviates from what is investments in additional production capacity. Could one use
considered optimal in terms of shape, size, and color such as the same thinking e.g., nega- foods for food security and
curved cucumbers, wrong sized apples being discarded sustainability? An investment in reducing the amount of foods
during lost or wasted (source reduction) will be just as valuable as an
sorting operations; investment in additional food production capacity. Hence,
• Foods that are close to, at or beyond the “best-before” dates source reduction by reducing food losses and waste from farm
are discarded by retailers and consumers; to fork will be necessary part of the future solution to feed 10
• Large quantities of wholesome edible food are often billion people sustainably.
left over and discarded from households and catering
establishments; and
Source Reduction—Using Novel IT and AI
• Producer or retailer recall of foods.
Solutions
These recalled foods might present a risk for a minority of the To achieve sustainability we must eliminate food losses and
population for example by containing allergens e.g., nuts. The waste. This proposition aligns well with the goals for reducing
recalled foods will be safe for the majority of the population resource and environmental footprints. On the other hand,
not allergic to nuts. Unspecific food recalls increase food the consumers wish to purchase their wanted food whenever
waste. In the United States, it was found that out of 382 recalls is convenient. Food businesses have difficulties in getting
42% was due to undeclared allergens (milk, nuts, eggs, soy, and their inventory policies right—when to reorder foods and the
wheat), 18% due to presence of food borne pathogens (e.g., appropriate stock levels to be maintained. In other words, food
Salmonella spp., Listeria spp. and E. coli), and 7% due to businesses, and retailers have a dynamic resource allocation
presence of foreign material (plastic and metal pieces; problem—the concurrent challenges of avoiding food waste
Maberry, 2019). and stock-outs. Food waste and stock-outs occur mainly
due to inaccurate forecasting of sales with the consequent
Assessment of Different Options for incorrect ordering of products (Arunraj and Ahrens, 2015).
Reducing Food Loss and Waste The factors correlated with the demand for foodstuffs in
The United States Environmental Protection Agency (EPA) retail stores include price, weather, season, events or festivals,
(2019) has described a hierarchy of options for reducing food promotions, or discounts in the store or competing stores,
losses and waste (Figure 1), that aligns well with the goals products characteristics (shelf life), and number of customer
of sustainability. Mourad (2016) compared the approaches of visits. Moreover, the time series of sales in food retail have
France and United States to food waste prevention. Her main high volatility and skewness varying over time, thus violating
finding was the three competing hierarchies of solutions to several assumptions of the standard statistical models.
surplus food production based on environmental, economic, Could greater use of predictive models, machine learning,
and social justifications. Implementing strong food waste neural networks and expert systems (artificial intelligence
prevention strategies such as changing the acceptance criteria or AI) enable the food business operators, to predict the
for fresh produce (ugly cucumbers) instead of weak prevention demand for food? Could fine-tuning the supply operations and
strategies (developing new best practices of food business demand forecasts, minimize stock-outs, and food waste? By
operators) could achieve more in terms of long-term using seasonal autoregressive, forecasting models with integrated
sustainability. While the aims of reducing food losses and moving averages with external variables model one could forecast
waste are highly desirable, food safety should be included in reasonably the daily sales of perishable foods (Arunraj and
this pursuit. The trade- offs, judgmental decisions taken, Ahrens, 2015). The forecast accuracies would improve if two or
should be evidence based and transparently justified. more models with different analytical approaches are used. For
example by combining moving averages with back propagation
neural networks, one could predict better the demand for
SOURCE REDUCTION—REDUCE WASTE fresh food in convenience stores (Chen-Yuan et al., 2010).
AND LOSSES Furthermore, food supplies could be better predicted by using
big data approaches such as data based on remote sensing—
Food Security an Insurance Question? metrology, images, genetic information, as well as laboratory
We need novel ways of looking at the food security and results and historical production data (Gounden et al., 2015).
sustainability. One consequence of such a shift in perspective
In this regard, Bayesian networks would be a more transparent
is that the food policy should focus on achieving zero hunger
method enabling better understanding and insights of the food
and good nutrition, and not on food production. Changing the
supply chain compared with machine learning approaches. One
perspective could open new ways of thinking about food and

Frontiers in Sustainable Food Systems | www.frontiersin.org 5 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

major concern is that food safety and quality considerations whole shelf life, for ready-to-eat foods able to support the growth
should be included into these promising big data models, to
obtain the full benefits.
There are complementary and competing visions for safe food
in the big data era (Nychas et al., 2016; Ropodi et al., 2016).
Multidisciplinary approaches should give the food industry better
tools for ensuring food quality and safety (Ropodi et al., 2016).
Possible methods for real time analyses of these huge data sets
include complicated and not very transparent algorithms such
as machine learning and computational intelligence (Ropodi et
al., 2016). The lack of transparency means that interpretation
of the results and giving evidence-based recommendations are
difficult. Moreover, the naïve application of forecasting of food
supply and demand, as well as monitoring the food chain
from farm to fork while ignoring food safety concerns, could be
a recipe for disaster. Hence, the big data strategies should
include food safety considerations. The benefits could be
reduction of food waste, ensuring food safety through a more
efficient control of the processes, and reassuring trust between
consumers and the food industry. Moreover, a move from
invasive or destructive testing toward non-invasive automated
monitoring based on sensors would be beneficial. These sensors
are easily implemented on-site, and will monitor production in
real-time. The massive amounts of high-throughput, analytical,
and imaging metadata collected with these instruments will
provide a holistic view of the spoilage and decaying processes of
the various food products across diverse storage conditions
(temperature and packaging) thereby better predicting food
supply. The online availability of this growing knowledge could
provide continuous benefits for the food industry. Big data
analyses promise a way forward to achieve the better
sustainability by reducing food loss and waste while also
ensuring food safety and quality.

Source Reduction by Intelligent Labeling Shelf


Lives “Best Before Date” and “Use by Date” The shelf life
of foodstuffs is labeled either as “best before dates” or “use by
dates.” The “best before date” is a food quality
management tool. The food business operator guarantees that
foods consumed before the best before date, is of good quality
provided the storage instructions are followed e.g., cold, dark
storage. After the best before date the food is safe but the quality
may decline. The consumer might deem the food as unsuitable
and unsafe, and consequently throw the food in the waste bin.
This is due to consumers confusing the “best before dates”
with “use by dates” intepreting both as “poisonous thereafter
dates.”
The “use by date” is a food safety management tool, indicating
the food is safe to eat until the’ use by date’, provided the food is
stored in compliance to the food business operators’ instructions.
The food business operator guarantees the food safety until
the “use by date.” Thereafter consumers should discard the
food. The foodstuff must comply with the end-product
microbiological safety criteria on the last “use by date.” Hence,
these criteria will determine the shelf life of a foodstuff. In the
European Union (EU), the microbiological safety criteria are
legally binding
[Commission Regulation (EC) No 2073/2005]. For example, the
number of listeria should be <100 c.f.u., per gram during the

Frontiers in Sustainable Food Systems | www.frontiersin.org 6 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs
of L. monocytogenes. However complicating the discussion,
there are great differences in susceptibility between healthy
and immuno-compromised groups (Rocourt et al., 2003) as
listeriosis is primarily a disease of those with impaired or
altered immune function (e.g., pregnant women and their
fetuses, the elderly, cancer patients, or patients being
immunosuppressed). Persons having organ transplants, being
pregnant, and persons undergoing dialysis are nearly 3,000,
1,000, and 500 times more likely to catch listeriosis than the
normal person, respectively (FAO/WHO, 2001). Further
increasing the disease burden is the fact that one out of
seven listeriosis cases is pregnant women (Desai and Smith,
2017). In the future, could one differentiate the shelf lives for
consumers by use of intelligent packaging and sensors? Could
those susceptible to listeriosis download an app on their
smartphone and scan the label on the food that could
indicate whether eating the food presents a risk. This app
could potentially reduce the amount of discarded foods and
food waste.

Intelligent Labeling and Sensors


Intelligent packaging and use of sensors have great
potential for reducing food waste and thereby improving
food security (Newsome et al., 2014; Poyatos-Racinero et al.,
2018). There are four families of sensors—for freshness, food
package integrity usually gas sensors, time-temperature
indicators (TTI), and identification tags such as radio-
frequency identification (RFID; Poyatos-Racinero et al., 2018).
The TTIs’ are helpful for detecting temperature abuse
along the distribution chain, and could permit dynamic
dating of a foodstuff’s shelf life. One could foresee
replacing the “use by dates” by e.g., a TTI indicator turning
red if the foodstuff is not suitable for human consumption or
yellow if the food quality declines. The freshness indicators
monitor the freshness by reacting to metabolites generated
by the foodstuff. Such indicators include organic acids, pH,
biogenic amines, ammonia, and/or carbon dioxide. The
freshness indicators need calibration for each foodstuff. Those
indicators suitable for freshness of leafy greens may not be
suitable for fish products. The gas sensors can check the
integrity of the food packaging, leakages of protective
atmospheres, or changes in gas metabolites (Ghani et al.,
2016). To make sensor a commercially viable proposition,
they need to be low cost, reusable, reversible, and long
lasting. Probably more difficult could be to educate
consumers on the meaning of the sensor outputs.
The RFID tags are helpful for tracing and tracking a food
product as it provides real time information on the food
product identity and the food chain. Moreover, the RFID tags
could provide data for analyzing the causes of food waste and
losses. An additional benefit could be in controlling food
frauds. Food frauds and fraudulent inputs in the food production
has emerged as an issue in recent years (Manning and Soon,
2016). In foods subject to fraud, RFID tags coupled with
block-chains could verify the origin and fate of the food.
Block-chains are tamper and fraud resistant and could thus
facilitate safe trade and reduce paperwork (Ahmed and
Broek, 2017). The trace- back when investigating outbreaks
will be faster and more precise when using block-chains.
Thus, one could target food recalls precisely. An important
element of food security is
Frontiers in Sustainable Food Systems | www.frontiersin.org 7 February 2020 | Volume 4 | Article 16
Vågsholm et Food Security, Safety, Sustainability Trade-Offs

the ability of governments to mitigate famines by importing disease prevention could be a very important contribution to
foods from other areas. Trust in the safety of foods is vital sustainable development in low and medium income countries
and use of block-chains could facilitate trust and speed up (McDermott et al., 2010).
the procedures.
Could one develop an alternative to large unspecific food Antimicrobials in Food Production—A Case of
recalls due to allergens, by sending allergic consumers or those Unsustainable Intensification
with specific food preferences (i.e., vegetarians or avoiding Antimicrobials has been used to intensify animal production by
pork) information through mobile phone apps enabling improving feed conversion and growth of the animals i.e., zoo-
avoiding certain foods by scanning the food labels? This would technical use. This approach was linked to large industrial
allowing consumers to check the foods in real time on the spot. animal production systems in which antimicrobials was an
The food businesses could then update these smartphone apps input to the production (Aarestrup and Wegner, 1999). When
instead of recalling the foods. This should also be simpler and Sweden joined the EU in 1995, one of the controversies was
enable more rapid spread of critical information. Those not the Swedish ban on zoo-technical use of antimicrobials. The
allergic or having particular food preferences could eat the Swedish Commission on Antimicrobial Feed Additives
food and consequently less food is wasted. (Commission on Antimicrobial Feed Additives. Antimicrobial
feed additives. SOU, 1997) concluded that whilst the use of
antimicrobials could intensify animal production and thereby
Source Reduction—Reduce Food Losses by
decrease footprints; these gains could not match the negative
Intensification of Food Production impacts of the consequent antimicrobial resistances (AMR).
The intensification of food production must align with the Animal production and welfare will be more sustainably
requirements for long-term sustainability (Rockström et al., maintained by implementing good husbandry, biosecurity, and
2017). The long-term sustainable agriculture has to operate preventive medicine than by using antimicrobials. More than
within its environmental boundaries to remain sustainable. 20 years later, the EU has banned the use of antimicrobials for
The key considerations of this approach include the ecological growth promotion and prophylaxis when the Regulation (EU)
dimensions, resource footprints and resilience, the social 2019/4 came into force. In plant production (Vidaver, 2002)
dimension of food security, and improving livelihoods of the the antimicrobials used are streptomycin and tetracycline,
global food production systems. Agriculture and aquaculture mainly as spray treatments of orchards. It appears that
food production should change from being a driver of global resistance to streptomycin has become widespread among
climate and environmental change to be the basis for global bacterial plant pathogens, illustrating the generic problem of
sustainability. In particular, food security resilience or the using antimicrobials as productivity enhancers (Vidaver, 2002).
ability to deal with shocks and stress in food production and Hence, we need alternative options to antimicrobials in plant
distribution without increasing the risks of hunger, malnutrition production including biocontrol agents, disinfectants, and
or food borne diseases, is critical. The double challenges of resistant plants.
shrinking arable land and increasing global population will
necessitate a smart intensification of food production (AT Food as Vehicle for Spreading Resistant Bacteria Hence,
Kearney, 2019). For example, more than half of the edible today AMR is a silent pandemic (Jasovský et al., 2016) for
vegetable production is lost in the fields (Johnson et al., 2018). which the use of antimicrobials in food production is a major
The losses are caused by failures of the harvest process, driver globally. Detection of antimicrobial substances in
failures to comply with supermarket specifications (wrong foodstuffs is uncommon while the findings of bacteria with genes
shape of cucumbers), or uneven ripening of the crops. This for AMR are frequent events. For example, in Sweden, 1395
indicates a straightforward way of increasing the amount of samples were taken in 2016 from animal foods (meat, dairy,
supplied foods and improved food security with limited egg, fish, and honey) and only one sample was positive for
downside risks including food safety. Moreover, the antimicrobial substances [National Food Agency (NFA), 2018].
sustainability would improve as the doubling of the amounts of Moreover, the import controls did not detect antimicrobial
plant foods available to consumers would require the same residues when sampling 3,693 consignments of foodstuffs
resource footprints i.e., inputs in terms of fertilizer, labor, originating outside EU. In contrast, between 10 and 55% of
irrigation water, and chemicals. Another approach could be the broiler carcasses were contaminated with extended spectrum
shifting to novel animal proteins derived from insects fed food beta-laktamase producing enterobacteria (ESBL) during the
waste and by-products that could replace traditional meat monitoring of broilers at slaughter between 2010 and 2018
products. A third approach to improve resilience is going down (Swedres-Svarm, 2018).
the food chain by eating the cereals today intended as animal The Biological Hazards panels of the European Food Safety
feedstuffs. The sustainability and food security would improve Authority (EFSA) published two opinions in 2008 and 2013
if animal production were based on feeds not available for [EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards),
human consumption i.e., pastures and grasslands. This would 2008, 2013] on AMR as a food borne hazard. The opinion
mean that pastoral production of beef, mutton and milk could from 2008 was a self-task opinion—a tool for EFSA scientific
be a very important contribution to the supply of high quality panels to warn about food safety risks. Could food could as a
proteins that ensures future food security. The intensification vehicle for human exposure to AMR bacteria and could one
of animal production derived from better animal nutrition, rank the identified risks and control options were the terms of
health and

Frontiers in Sustainable Food Systems | www.frontiersin.org 8 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

reference. The second opinion was on carbapenems i.e., broad- which in the case of “use-by dates” could indicate an increased
spectrum β-lactam antimicrobials used for the treatment of risk for food borne disease or “best before dates” of possible
serious infections in humans and the presence of resistance in decreased quality.
animals. Both opinions noted that foodborne pathogens and
commensals display diverse ranges of resistance to Food Donations—Liability Concerns
antimicrobial agents of human and veterinary importance. Spread Could liability concerns impair the willingness to donate or
of resistance amongst bacteria in foods will influence public redistribute foods? For example, Austrian supermarkets
health. For example, the bacteria resistant to fluoroquinolones as discard around 10% of the bread (Lebersorger and Schneider,
well as 3rd 2014). Of these discarded breads, only 7 % is donated to food
and 4th generation cephalosporin being found in a variety of banks i.e., < 1% of total bread production. One reason for this
foods and in animals in primary production. The major source
is the concerns of food business operators about their liability
of human exposure to fluoroquinolone resistance via food was
when donating perishable foods that might be associated with
poultry, whereas for cephalosporin resistance the sources were
foodborne disease. To ease such liability concerns, USA and Italy
poultry, pork and beef.
have implemented
Good Samaritan Laws. These laws protect donors from liability
Future Perspectives on Control of AMR in Food
when donating to non-profit organization as well as from civil
To be sustainable the intensification of food production
and criminal liability if a product, donated in good faith, later
systems (Rockström et al., 2017) must incorporate the control
causes harm to one of the needy beneficiaries (Braun, 2010).
of AMR. The EFSA opinion [EFSA BIOHAZ Panel (EFSA Panel on
To encourage food donations and use of food banks, one will
Biological Hazards), 2008] suggested monitoring and
need legislation on how to donate food without incurring
restrictions of antimicrobial use in food animals, and a focus on
liabilities.
pre- harvest control. This aligns well with the US Food
and Drug Administration’s (FDA) action plan on Food Donations—Resilience and Novel IT Solutions Food
antimicrobial drug steward ship (FDA/CVM, 2018). FDA donation programs and food banks will help to mitigate food
concluded that medically important antimicrobial drugs should insecurities (EFSA AHAW Panel, 2006). If these programs are
not be used for zootechnical purposes in food animals or as well-designed and run they will prevent starvation and thereby
over the counter (OTC) drugs. Moreover, the Food and enhance welfare for socioeconomic disadvantaged groups.
Agriculture Organization’s (FAO) action plan on FAO (2016) This will improve the sustainability, resilience, and stability of
suggested improving (a) global awareness of risk factors for a society. The typical donations to food banks are non-
AMR emergence and spread, (b) improve monitoring of perishable foods such as canned, frozen, and dry foodstuffs.
antimicrobial use and AMR, Food banks could also be in the form of rescue programs
(c) strengthen the governance related to AMR in foodstuffs such as community shelters, soup kitchens, and food pantries
and agriculture, and (d) promote good practices and prudent where perishable and non-perishable foods are distributed. Food
use. WHO (2015) noted that a One Health approach and banks are important for easing acute food deprivation and
political will are prerequisites for tackling the challenge of risk of hunger (Bazerghi et al., 2016). On the other hand,
AMR. In the future, one should reserve the remaining efficient food banks may have limited ability to improve the nutritional
antimicrobials for treating human infections. These insights status of the recipients due to the limited supply of nutrient-
have major implications for veterinary medicine and animal dense and perishable foods such as dairy, vegetables, and
science including: fruits. Nevertheless, the contributions to food security will be
• Antimicrobial drugs should not substitute for substandard considerable if the food banks address their clients’ nutritional
rearing facilities and animal welfare, needs and provisions of perishable foods are available.
• Great need for improved preventive medicine, Moreover, food banks have usually limited economic
• Better vaccines to protect against infections, resources for transportation and storage of foods. The biggest
• Food production systems with better biosecurity and animal challenge for food banks are predicting their food supplies, which
health and welfare, impair their ability to transport, store, and distribute donated
• Animal breeding program aimed at robustness and foods cost efficiently (Brock and Davis, 2015). Moreover, to
resilience; and ensure a wholesome diet for their clients the food banks often
• The development of separate veterinary and need to purchase complementary foods. Novel IT and artificial
human antimicrobial substances based on different intelligence solutions such as multilayer perceptron neural
biological mechanisms. networks (MLP-NN) appear best suited to predict the dynamics
of food supplies. This is another example how novel solutions like
artificial intelligence could help limiting the food waste.
REDISTRIBUTE OR REPROCESS FOOD
Food Donations and Food Safety
One can redistributed food through food banks and food Compared with conventional food chains, food donation chains
donation programs. These are both examples of urban mining are often less structured and with incomplete cold chains (De
(Schneider, 2013). These measures may be important to make the Boeck et al., 2017). Another concern is the frequent lack of
food available to disadvantaged socioeconomic groups. Typically, food hygiene training of those working with food donations.
the donated foods are closer to the end of their shelf lives, The donated perishable foods are mostly ready to eat or
Frontiers in Sustainable Food Systems | www.frontiersin.org 9 February 2020 | Volume 4 | Article 16
Vågsholm et Food Security, Safety, Sustainability Trade-Offs

ready to be reheated meals. When analyzing 72 samples from linked to quality and spoilage problems in the dairy industry
perishable foodstuffs taken from social groceries in Belgium, contributing to food losses since it survives pasteurization
increased numbers of listeria monocytogenes (log 3.5 CFU/g) (Andersson et al., 1995). While reprocessing food is beneficial
and enterobacter (6.7 CFU/g) were found in ready-to-eat from food security and sustainability perspectives, one must
cooked meat (Wooldridge et al., 2006). It highlights the need avoid negative trade-offs with food safety. Hence, training of
for sufficient cooling capacity if food banks intend to accept the food business operators involved in food reprocessing is a
perishable foods. Another concern is that people eating strong recommendation.
donated foods are often more susceptible to catch food borne
diseases due to other co-morbidities or health conditions,
indicating the need for careful trade-offs between food safety
RECYCLE
and mitigating food insecurity. In conclusion, for food donation
programs to work food safety is a prerequisite. Reprocess Wasted and Lost Food to Feed
Animals
Can we manage the trade-offs when developing circular food
Reprocessing Foodstuffs for Human production systems based on reprocessing foodstuffs to animal
Consumption feed? One conclusion is that the management of these trade-offs
Reprocessing often means that foodstuffs reaching their “best should be evidence based and balance carefully the costs, risks
before dates” or “use by dates” are reheated or frozen. For and benefits to food safety, security, and sustainability. The worry
example, salmon filets and beef pieces are minced into salmon is that the recycling of nutrients could result in the recycling
or beef patties, and thereafter fried for another shelf life. Another of biological and chemical hazards. For example, EFSA AHAW
option is freezing foods just before their best before or use by Panel (2006) concluded on the use of dairy byproducts such as
dates. A third option is to use food leftovers as raw materials raw milk, white water, or unpasteurized dairy products as feed
for next meals or reheat the leftovers. A study of Swedish for animals could present risks for transmission of biological
supermarkets (Lagerberg Fogelberg et al., 2011) found that for hazards. The EFSA opinion identified 24 hazards as animal
the supermarket having its own chef making warm lunches or pathogens including four zoonoses. Animal pathogens such as
dinner portions was a paying proposition. The amounts of food Foot and Mouth Disease virus (FMDV) present a threat to
waste were reduced as foodstuffs nearing the “best before date” animal health and thereby to food security, while zoonoses like
or with any visible signs linked to lesser consumer acceptance, Q-fever, brucellosis and salmonellosis, in addition present a
were processed into warm lunches, pates or pies, and ready threat to food safety and public health. Hence, in reprocessing
to eat sandwiches. In addition, customers got better service, foods there should be treatment steps that eliminates the
and the supermarkets got another business opportunity. That relevant pathogens. For example, feeding wasted or lost
foods intended for the bin, were processed into meals to be foodstuffs as e.g., scraps to pigs is an old way of taking care
sold appeared to improve the profits. The supermarkets reported of the nutrients to maintain and improve the food supply and
moreover, that employing a chef enhanced the hygiene standards sustainability (Salemdeeb et al., 2017). Historically, pigs were
amongst the other employees. living storages of food for people when food spoilage were the
Reheating already prepared dishes improve food supply big problem. On the other hand, feeding pigs scraps could
but includes a food safety risk. The classic example is spread diseases such as Classical Swine Fever, African Swine
the growth of toxin producing bacteria linked to the slow Fever, Swine Vesicular Disease, and, Foot and Mouth Disease
cooling of and thereafter reheating of pea soup (Nyberg and (Wooldridge et al., 2006).
Lindqvist, 2017). For example in Sweden around 20% of the For lost or wasted plant foodstuffs, recycling, and reprocessing
reported cases of food borne diseases were associated with food as animal feed should be easier as fewer of the concerns
toxin producing bacteria—Staphylococcus aureus, Clostridium about transmitting animal disease or zoonotic pathogens apply.
perfringens, and Bacillus cereus (Lindqvist, 2019), while the The BSE epidemic caused the tightened controls of feed
European Food Safety Authority (EFSA) reported that a similar producers reprocessing plant food in the European Union and
proportion of the food borne outbreaks in EU during 2018 feeding scraps to food animals was prohibited. All feed producers
were linked to bacterial toxins−18.5% (EFSA (European Food processing food waste of plant origin to animal feed must
Safety Authority), 2019). Staphyloccus aureus food poisoning is be officially supervised. Thus, feeding the neighbor’s pig some
associated with cross contamination and thereafter temperature pieces of bread is a regulated activity. One side effect of these
abuse of foodstuffs kept between 5◦ and 60◦C (Hennekinne prohibitions has been the limits on circular and thereby more
et al., 2012). The latter two species are spore forming and sustainable animal production systems. Consequently, of
the spores survive cooking or similar heat treatments. For nearly 100 million tons of food waste only 3 million tons are
example, C. perfringens foodborne intoxications are linked to recycled as animal feed (Salemdeeb et al., 2017). There are
slowly cooling and reheating dishes with meat such as pea several benefits from substituting feedstuffs based on cereals or
soup (Andersson et al., 1995; Nyberg and Lindqvist, 2017). In soybeans with plant based food scraps in terms of resource
a similar way, insufficiently heated (typically not hot enough footprints, sustainability, and amounts of heavy metals
water baths) rice dishes are linked to B. cereus food poisoning entering the food chains. Moreover, the costs to farmers of
(Andersson et al., 1995). In the dairy industry B. cereus is feeding their animals recycled foods are more predictable than
of feedstuffs where prices determined by a volatile market. In
conclusion, getting
Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16
Vågsholm et Food Security, Safety, Sustainability Trade-Offs

this trade-off right could unlock substantial benefits and profits acids to the water after the bio-filter, the pH is lowered to 5–6
to consumers and farmers, respectively. to optimize the uptake

Recycle Through Insects


A novel way would be to feed insects e.g., house crickets
(Acheta domesticus) with wasted or lost foodstuffs with a view
of eating the insects or feeding them to animals. However,
following food safety and quality concerns were identified
(Fernandez-Cassi et al., 2019):
• High total counts of aerobic bacteria meaning that spoilage will
be rapid unless there is a heat treatment step soon after
harvest;
• The presence of spore-forming bacteria after heat treatment
with the implication that insect based foods with slow
cooling after heat treatment could have high numbers of these
bacteria;
• The accumulation of cadmium and other heavy metals
necessitating controls of the feed given to insects; and
• The possible increase of allergenic reactions due to exposure
to insects and insect derived products, this could increase
risk of product recalls.
Perhaps more important were the data gaps leading to high
levels of uncertainty when considering trade-offs. These data
gaps include lack of knowledge on the farming conditions of
the insects, the breeding pyramids, and the impact of thermal
processing of the products prior to consumption. For example,
what could be the impact of mycotoxin-producing fungi, a
likely proposition since the crickets are foreseen reared in hot
and humid conditions? Could heat-treating the insects imply
risks from chemical hazards such as heterocyclic aromatic
amines or acrylamide? Hence when introducing novel foods
that are very promising from sustainability and food security
perspectives, we need sufficient evidence for managing the
food safety risks.

Circular Food Production—Aquaculture and


Aquaponics
Circular food systems are very efficient in terms of environmental
and resource footprints. Circular systems means that most of
the nutrients are recycled, but unless there sufficient hurdles
such as species barriers this cycle of nutrients can become a
cycle of pathogens or chemical hazards. This means that the
biosecurity and possible hurdles of circular food production
systems should receive special attention. One example of
a circular food production system is the combination of
aquaculture and aquaponics (Monsees et al., 2017).
Aquaculture has environmental benefits compared with animal
production on land such as smaller water footprints and better
feed- conversion approaching 1 kg of feed to 1 kg of fish meat. A
combined aquaponics and aquaculture based food production
system could further minimize the environmental footprints
since the waste produced by the fish are fertilizing plants.
However, circular food productions systems have their own
challenges. The fish metabolism produces ammonia that in the
bio-filters are converted to nitrates. This conversion of
ammonia to nitrates requires the pH to be kept above 7
that subjects the fish suboptimal rearing conditions with
consequent health and welfare risks. Thereafter by adding

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs
of nutrients by the plants when used for irrigation. Hence,
for fish welfare and health reasons decoupling the aquaponics
and aquaculture systems could be beneficial. Moreover, the
yields from separately optimized aquaponics and aquaculture
production systems appear to be higher than for coupled
systems.

Circular Food Systems—Benefits and Risks


Circular food systems had the potential to reduce food waste
and losses and thereby improve the sustainability of the food
systems and food security (Jurgilevich et al., 2016). Today the
sustainability of our food security is challenged since between
30 and 50% of the food is lost or wasted in different
stages of the food system, with consequent higher
consumption of animal foodstuffs and larger environmental
footprints. Circular food production systems will imply
smaller environmental and resource footprints and the
recycling of nutrients, by- products and food waste, resulting in
less food waste, and losses. An additional benefit is the
improved transparency possible from shorter and local food
chains. Combining local and seasonal elements in supply
chains could improve the balance of food supply and demand
and reduce needs for storage and transportation. On the
other hand, there are risks when making the transition from a
linear extractive food production system to a circular and
recycling one. Slaughterhouses produce a lot of food waste
for example offal, specified risk material (SRM), condemned
parts of carcasses or condemned whole carcasses. Approval
or condemnation of carcasses is necessary food safety
procedure, but too frequent condemnation contributes to
additional food waste (Arzoomand et al., 2019). One of the
reasons for this excess condemnation is the lack of training of
the meat inspector and slaughterhouse staff. Previously, the
waste and by-products from slaughterhouses were rendered
into meat and bone meal (MBM) to recover the high quality
nutrients for animal feed. Could such a cycle of nutrients also
could become a cycle of pathogens?

BSE Outbreak and the Risks From Circular Food Systems


One example of a failed circular food production system
was the outbreak of mad cow disease (Bovine Spongiform
Encephalopathy—BSE; Ducrot et al., 2008). BSE is one of
the diseases called Transmissible Spongiform
Encephalopathies (TSEs) affecting the brain and nervous
system of humans and animals, all caused by abnormal forms
of proteins (prions). BSE is a zoonotic disease in cattle
causing variant Creutzfeldt- Jakob’s disease (vCJD) in people
(Bruce et al., 1997). In the European Union, between 1996
and 2013, 226 cases of VCJD were detected of which 177 was
detected in in UK (European Center for Disease Control,
2019). In cattle from 1987 to 2014, 190,182 cases of BSE
were detected of which 184,637 cases in UK (European
Commission, 2015). One BSE infected cow could infect 15–20
other cows through the rendering, MBM and ruminant feed
cycle (De Koeijer et al., 2004), thus illustrating the disease
transmission potential of circular food production systems
when they fail. Could lessons learned from the BSE and
vCJD outbreak inform the design of future circular food
production systems? It is worth remembering that the
rendering

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

of offal from slaughter to protein and energy concentrates persons, or around 30.000 carriers in total in UK, in contrast to
intended for feeding to animals was good husbandry practice the 177 vCJD cases reported to date (Gill et al., 2013).
until 1988 (ARC (Agricultural Research Council), 1980). These
practices included feeding calves and dairy cows with ruminant Take Home Lessons BSE Epidemic
meat and bone meal (MBM) in milk replacers and in In retrospect, while BSE epidemic was a huge outbreak in cattle
concentrate feedstuffs. When the rendering temperature, time and tragedy for society, the actual public health impact was
and pressure were reduced and the ether extraction of fats were smaller than for many other food borne diseases. Another
discontinued, the circulation of the prions became possible. The lesson was that dealing with the fear of a huge disease
reasons for these changes in rendering process were: increased outbreak and resultant loss of trust, might be just as difficult as
demands for high nutrient feedstuffs due to increasing yields in dealing with an actual outbreak. A particular challenge was that
dairy production, cost pressures—feeding the cheapest protein when BSE emerged as a cattle disease, the causes for this
feed ingredients, the aims of reducing animal waste and by- emergence emerged around 5 years earlier. Furthermore, the
products and reducing the environmental footprints, and food control measures implemented would give results after lag
security and self-sufficiency (Ducrot et al., 2008). period of 5 years. Explaining this lag between control actions
According to the UK BSE Inquiry (The inquiry into BSE and seeing results to decision makers and the public was
Variant CJD of the United Kingdom, 2002) the first cases were difficult. Moreover, the ability BSE to spread amongst cattle
noted in December 1984, while the official recognition of the and thereafter to other species indicating the zoonotic risks
new cattle disease as BSE was 2 years later. In 1988 the results was first grasped when thinking in One Health perspectives.
epidemiological and pathological studies (Wilesmith et al., Another insight was that the good functioning of the internal
1988) established that ruminant MBM was a risk factor for BSE. market for food in the EU is contingent on the consumers’ trust
Consequently, feeding cattle with ruminant MBM was prohibited in the management of food safety risks, and that the loss of
in the summer of 1988. In addition, BSE became notifiable, public confidence can be difficult to repair. Hence, the public
and a stamping out policy for cattle showing clinical symptoms confidence in the food safety is critical for sustainable and
were introduced. In 1989 Specified Bovine Offal (SBO) e.g., the resilient food production systems. When designing circular
brains and spinal cords, eyes but later extended to distal ileum food production systems one priority must be avoiding cycles
and spleen) were prohibited from human consumption, and of biological and chemical hazards. One surprise to remember
pet manufactures ceased voluntary to use of SBO. In was the higher persistence of prions (BSE pathogen) in the food
retrospect, it appeared that the number of BSE infected cows and feed chains compared with the pathogens thought to be
decreased for each annual cohort borne 1988 and thereafter present in 1980s.
indicating the efficiency of the control measures (Ducrot et al.,
2008). The BSE outbreak became a crisis in 1996 when BSE was RECOVER AS BIOFUEL AND NUTRIENTS
designated as a zoonosis (Bruce et al., 1997). The BSE
epidemic in UK peaked in 1992/93 4 years after control Here the strategy is to recover the energy and use as fertilizers the
measures were implemented as a consequence of the nutrients from food losses and wastes as well as byproducts from
incubation period of BSE being 4–6 years (Doherr, 2007). animals and vegetable food production. These recover
Due to this delayed peak, the rest of European Union (EU) strategies are less favorable in terms of food security and
member states considered from 1988 to 1993 that BSE was a sustainability than the previously discussed strategies. On
UK problem. The consequence was the EU member states the other hand, as complements they could be valuable. Even
delayed implementing control measures in their food chains. here there are trade-offs between food safety, sustainability and
During these years, UK exported ruminant MBM to the rest of food security.
Europe as protein ingredients for poultry and pig feed
production (Ducrot et al., 2008) as well as calves and heifers. Recover Biogas and Nutrients From Manure
These exports were the drivers for the next wave of BSE that One complementary approach is the recycling of manure from
emerged in several EU countries (Doherr, 2007). BSE cases animal production (Leibler et al., 2017) for industrial uses to
were diagnosed in Ireland 1989, in Switzerland 1990 and in recover the energy and recover the nutrients as fertilizers.
France 1991. However, it was first in 1994 that EU imposed a Here it is a possible win-win situation for sustainability and
mammalian MBM ban to cattle all over EU. EU extended this ban food security, but with risks for food safety. The amounts of
in 2001 to a complete ban of MBM fed to food animals in EU. The manure from animal production such as poultry and pig farms
BSE geographical risk assessments predicted that countries that are often concentrated on small areas. Hence, there might
having imported cattle and MBM from UK was at higher risk in be risks of releases of pathogens such as the avian flu virus. The
particular if their rendering and feeding practices enabled the avian flu virus might survive up to 600 days in manure (Graiver
BSE to circulate (European Commission, 2003; Salman et al., et al., 2009) creating a potential hot spot for transmission or
2012). The public health concerns were elevated as modeling later re- emergence of the disease if the manure is left
studies predicted up to 1 million persons in UK were incubating untreated. The food waste residues after biogas production
vCJD (Cousens et al., 1997; Ghani et al., 1998). These modeling could be valuable as fertilizers and lowering the resource
results were revisited later (Smith et al., 2010) by studying the footprint of food production. Composting, anaerobic digestion,
prevalence of abnormal prion protein in appendixes, indicating and ammonia treatment are three methods for recovering
a prevalence of 1 carrier out of 2,000 nutrients and energy from bio- wastes and manure (Albihn and
Vinnerås, 2007), with different

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

advantages and disadvantages. For example, anaerobic digestion settings and a safety valve for more advanced sustainable
might produce biogas and degrade organic pollutants, while on food systems.
the downside there is the need for expensive high tech Landfills are unpopular, as most people do not want them
equipment. The selection of treatment methods should be on nearby. Landfills appear to be the least sustainable system for
case-by- case basis, but the key parameters for controlling taking care of food waste () having the largest environmental and
pathogens in producing fertilizers were the time temperature resource footprints. Moreover, the biosecurity and food safety
profiles and ammonia content. risks are important as landfills where food waste is dumped, tend
be populated by vermin. For example in Finland, an outbreak of
Recover Energy Through Biofuel trichinellosis could be linked invasion of rats from an
Production improperly closed dump nearby (Oivanen et al., 2000).
Biofuels include biogas, bioethanol, biodiesel and biobuthanol
(Tabatabaei et al., 2015). The choice of substrates for biofuel
production should be as wide as possible such as agricultural INSIGHTS AND CONCLUSIONS
and food industry losses and waste, household waste, and
solids from municipal wastewater. For example, EFSA reviewed Feeding 10 billion people in 2050 sustainably will require
the biosecurity of making biodiesel from animal by-products changes of our food chains. Changing of our food demand
such as fish oil, animal fats derived from offal [EFSA BIOHAZ to more plant based diets could help as half of the world’s
Panel (EFSA Panel on Biological Hazards), 2015]. Even fats from cereal production ends up as animal feed while only around
sewage cleaning facilities, cooking and frying oils were possible one third is for human nutrition (Willett et al., 2019). The
substrates. The current biosecurity requirement for the biodiesel future diets might align with recommendations of the EAT-
process is to reduce the infectivity of the BSE agent by at least one Lancet report (AT Kearney, 2019), but with local adaptions.
million times (log 6) in order to use all risk categories of offal as For example, the beef, mutton, and milk produced from
substrate. The sustainability gains originates from smaller climate pastoral farming systems will remain. The ecosystem benefits
footprints as biodiesel could substitute for kerosene to of open landscapes should give further incentives for pastoral
airplanes and for diesel to trucks and agricultural machines. farming practices. Moreover, seafood produced through
Another caveat for sustainability is that the substrates for farming and in circular systems could supply high quality
biofuel production should not be possible to use as human proteins wherever this production is feasible (Oivanen et al.,
food or animal feeds. In this regard, the emerging linkages 2000). Another major source of food supply could emerge if
between the oil and food prices (Al-Maadid et al., 2017) are a the 30% of food produced that is now lost or wasted, could
concern. Consequently, the prices of global staple foods such become available for human consumption. Source reduction
as cereals and sugar would go up if oil price increased. This and reprocessing of foods appears to be the best options
could be a major concern to social sustainability and food to eliminate food waste or loss. One example of sustainable
security as food prices become more volatile when edible intensification and source reduction could be intensifying the
foodstuffs are diverted into biofuel production to substitute for harvest of vegetable crops to double the output with the same
oil. footprint. This will require consumers and food businesses to
adapt their quality requirements and specifications (Johnson
et al., 2018). If the global food systems could change in this
INCINERATION AND LANDFILLS direction, the global food security will improve and be more
resilient. Using modern IT technology offers the best promise
Incineration and landfills are the least desirable strategies for of more efficient source reduction, reprocessing, and recycling
dealing with food waste and losses. However, incineration has of food.
some advantages from a sustainability perspective. In developing It is however, vital to get the trade-offs right between food
countries with energy poverty and where food waste is safety, food security and economic, social and environmental
dumped in unsanitary landfills, incineration to produce sustainability. These trade-offs should be evidence and risk
electricity and heat is an alternative that could improve based. Good intentions will not compensate for failures as
sustainability (Unaegbu and Baker, 2019). The food lost or shown by the failed use of antimicrobials to achieve food
wasted is already available as fuel and can replace oil used to security through intensifying food production. A veterinary
produce energy needed locally. The benefits are from medicine and food value chain not requiring antimicrobials
converting food waste into an energy and electricity resource is therefore a necessary aim for research and innovation. The
available locally. This would improve the resilience and make transition of animal production from intensive cereal based
cold chains a viable proposition in development settings. farming to more extensive pastoral farming will probably
Another example from Sweden is that if farmers or feed imply changes to veterinary medicine. For example, nutritional
mills have spoiled cereals due to mold, one could incinerate supplements and control of parasites may become bigger
the grains to recover the energy (SOU, 2007). Benefits include concerns than diseases related to rapid growth. In conclusion,
avoiding for sure those moldy grains enter the food or feed the trade-offs and subsequent decisions regarding food safety,
chains and green energy the foods already lost due to molds. food security, and sustainability are not trivial and should be
Hence, incineration could cut oil consumption and carbon evidence based.
footprints. Hence, one could think of incineration as starting
point in development

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

AUTHOR CONTRIBUTIONS to the slaughter and recycling of offal and the BSE epidemic,
assessing evidence, and the writing of the paper. SB
IV designed, searched and collated references, assessed evidence
contributed on the design of the paper, the issues of circular
in particular on source reduction, and wrote the paper. NA food production systems, antimicrobial resistance and
contributed on the issue of circular food system in reference sustainable intensification, and the writing of the paper.

REFERENCES De Koeijer, A., Heesterbeek, H., Schreuder, B., Oberthür, R., Wilesmith, J., van
Roermund, H., et al. (2004). Quantifying BSE control by calculating the basic
Aarestrup, F. M., and Wegner, H. C. (1999). The effects of antibiotic usage in reproduction ratio R0 for the infection among cattle. J. Math. Biol. 48, 1–22.
food animals on the development of antimicrobial resistance of importance doi: 10.1007/s00285-003-0206-x
for humans in Campylobacter and Escherichia coli. Microbes Infect. 1, 639– Desai, R. W., and Smith, M. A. (2017). Pregnancy-related listeriosis. Birth Defects
644. doi: 10.1016/s1286-4579(99)80064-1 Res. 109, 324–335. doi: 10.1002/bdr2.1012
Ahmed, S., and Broek, N. T. (2017). Food supply: block-chain could boost food Doherr, M. G. (2007). Brief review on the epidemiology of transmissible
security. Nature 550:43. doi: 10.1038/550043e spongiform encephalopathies (TSE). Vaccine 25, 5619–5624.
Albihn, A., and Vinnerås, B. (2007). Biosecurity and arable use of manure doi: 10.1016/j.vaccine.2006.10.059
and biowaste - treatment alternatives. Livestock Sci. 112, 232–239. Ducrot, C., Arnold, M., Koeijer, A., Heim, D., and Calavas, D. (2008). Review
doi: 10.1016/j.livsci.2007.09.015 on the epidemiology and dynamics of BSE epidemics. Vet. Res. 39:15.
Al-Maadid, A., Caporale, G. M., Spagnolo, F., and Spagnolo, N. (2017). Spillovers doi: 10.1051/vetres:2007053
between food and energy prices and structural breaks. Int. Econ. 150, 1–18. EFSA (European Food Safety Authority) (2019). Scientific report on the
doi: 10.1016/j.inteco.2016.06.005 European Union One Health 2018 Zoonoses Report. EFSA J. 17:5926.
Andersson, A., Ronner, U., and Granum, P. E. (1995). What problems does the doi: 10. 2903/j.efsa.2019.5926
food industry have with the spore-forming pathogens Bacillus cereus and EFSA AHAW Panel, 2006###EFSA AHAW Panel (2006). Opinion of the scientific
Clostridium perfringens? Int. J. Food Microbiol. 28, 145–155. panel on animal health and welfare on a request from the commission
ARC (Agricultural Research Council) (1980). The Nutrient Requirements of related to “the animal health risks of feeding animals with ready-to-use dairy
Ruminant Livestock. Slough: Commonwealth Agricultural Bureaux. products without further treatment”. EFSA J. 347, 1–21. doi:
Arezki, R., and Brückner, M. (2011). Food Prices and Political Instability. 10.2903/j.efsa.2006.347
IMF working paper. WP/11/62. IMF (Washington, DC). Available online EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards) (2008). Scientific
at: https://www.imf.org/en/Publications/WP/Issues/2016/12/31/Food-Prices- opinion of the panel on biological hazards on a request from the European Food
and-Political-Instability-24716 (accessed July 2, 2019). Safety Authority on foodborne antimicrobial resistance as a biological
Arunraj, N. S., and Ahrens, D. (2015). A hybrid seasonal autoregressive hazard. EFSA J. 765, 1–87. doi: 10.2903/j.efsa.2008.765
integrated moving average and quantile regression for daily food sales EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards) (2015). Scientific
forecasting. Int. J. Prod. Econ. 170, 321–335. doi: 10.1016/j.ijpe.2015.09.039 opinion on a continuous multiple-step catalytic hydro-treatment for
Arzoomand, N., Vågsholm, I., Niskanen, R., Johansson, A., and Comin, A. (2019). the processing of rendered animal fat (Category 1). EFSA J. 13:4307.
Flexible distribution of tasks in meat inspection – a pilot study. Food Control doi: 10.2903/j.efsa.2015.4307
102, 166–172. doi: 10.1016/j.foodcont.2019.03.010 EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards) (2013). Scientific
AT Kearney. (2019). How Will Cultured Meat and Meat Alternatives Disrupt the opinion on Carbapenem resistance in food animal ecosystems. EFSA J. 11:3501.
Agricultural and Food Industry?Dusseldorf; AT Kearney Studie zur Zukunft doi: 10.2903/j.efsa.2013.3501
des Fleischmarkts bis 2040. Available online at: https://www.atkearney.com/ Environmental Protection Agency (EPA) (2019). Sustainable Management
retail/article/?/a/how-will-cultured-meat-and-meat-alternatives-disrupt-the- Food. Available online at: https://www.epa.gov/sustainable-management-food
agricultural-and-food-industry (accessed July 5, 2019) (accessed March 1, 2019).
Bazerghi, C., McKay, F. H., and Dunn, M. (2016). The role of food banks in European Center for Disease Control (2019). Facts About Creutzfelt Jacob’s Disease.
addressing food insecurity: a systematic review. J. Community Health 41, Available online at: https://ecdc.europa.eu/en/vcjd/facts (accessed April 10,
732–40. doi: 10.1007/s10900-015-0147-5 2019).
Boqvist, S., Söderqvist, K., and Vågsholm, I. (2018). Food safety challenges and European Commission (2015). Transmissible Spongiform Encephalopathies
one health within Europe. Acta Vet. Scand. 60:1. doi: 10.1186/s13028-017-0355- (TSEs) in the EU in 2014. Available online at:
3 Braun, J. (2010). Food insecurity, hunger and malnutrition: necessary policy https://ec.europa.eu/food/sites/food/ files/safety/docs/biosafety_food-borne-
and disease_tse_ms-annual-report_2014. pdf (accessed April 10, 2019).
technology changes. N. Biotechnol. 27, 449–452. doi: 10.1016/j.nbt.2010.08.006 European Commission, Scientific Steering Committee (2003). The Scientific
Brock, L. G., and Davis, L. B. (2015). Estimating available supermarket Steering Committee (SSC): A Short History of Six Busy Years. Available online
commodities for food bank collection in the absence of information. Expert at: https://ec.europa.eu/food/sites/food/files/safety/docs/biosafety_food-
Syst. Appl. 42, 3450–3461. doi: 10.1016/j.eswa.2014.11.068 borne-disease_tse_ssc-history.pdf (accessed July 10, 2019).
Bruce, M. E., Will, R. G., Ironside, J., and McConnell, I. (1997). Transmissions to European Parliament (2017). Cutting Food Waste. Press Release
mice indicate that ’new variant’ CJD is caused by the BSE agent. Nature 389, 20170509IPR73930. Available online at: http://www.europarl.europa.eu/
498–501. doi: 10.1038/39057 news/en/press-room/20170509IPR73930/cutting-food-waste (accessed March
Chen-Yuan, C., Wan-I, L., Hui-Ming, K., Cheng-Wu, C., Kung-Hsing, C. (2010). 1, 2019).
The study of a forecasting sales model for fresh food. Expert Syst. Appl. 37, FAO (2011). Global Food Losses and Food Waste – Extent, Causes & Prevention.
7696–7702. doi: 10.1016/j.eswa.2010.04.072 Rome: FAO.
Commission on Antimicrobial Feed Additives. Antimicrobial feed additives. FAO (2012). State of the World’s Fisheries and Aquaculture. Rome: FAO.
SOU (1997). Swedish Government, Ministry of Enterprise and Innovation, FAO (2016). The FAO Action Plan on Antimicrobial Resistance 2016-2020. Rome:
Stockholm, Sweden. Available online at: https://www.government.se/legal- Food and Agriculture Organization of the United Nations. Available online at:
documents/1997/01/sou-1997132/ (accessed July 4, 2019). http://www.fao.org/3/a-i5996e.pdf (accessed Oct 14, 2019).
Cousens, S., Vynnycky, E., Zeidler, M., Will, R., and Smith, P. (1997). Predicting FAO/WHO (2001). Joint FAO/WHO Expert Consultation on Risk Assessment of
the CJD epidemic in humans. Nature 385, 197–198. Microbiological Hazards in Foods. Risk Characterization of Salmonella in Eggs
De Boeck, E., Jacxsens, L., Goubert, H., and Uyttendaele, M. (2017). Ensuring and Broilers and Listeria monocytogenes in Ready-to-Eat Foods. FAO Food
food safety in food donations: case study of the Belgian donation/acceptation and Nutrition Paper No. 72. Rome: Food and Agriculture Organization of the
chain. Food Res. Int. 100, 137–149. doi: 10.1016/j.foodres.2017.08.046 United Nations.

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16


Vågsholm et Food Security, Safety, Sustainability Trade-Offs

FDA/CVM (2018). Supporting Antimicrobial Stewardship in Veterinary Maberry, T. (2019). A Look Back at 2018 Food Recalls. Food Safety Magazine, E-
Settings – Goals for Fiscal years 2019-2023. Rockville, MD: Center for Newsletter, February 19. Available online at: https://www.foodsafetymagazine.
Veterinary Medicine Food and Drug Administration. Available online at: com/enewsletter/a-look-back-at-2018-food-recalls-outbreaks/ (accessed July
https://www.fda.gov/animal-veterinary/judicious-use-antimicrobials/fdas- 4, 2019).
cvm-key-initiatives-antimicrobial-stewardship (accessed October 11, 2019). Manning, L., and Soon, J. M. (2016). Food safety, food fraud, and food defense: a
Fernandez-Cassi, X., Supeanu, A., Vaga, M., Jansson, A., Boqvist, S., and fast evolving literature. J. Food Sci. 81, 823–834. doi: 10.1111/1750-3841.13256
Vagsholm, McDermott, J. J., Staal, S. J., Freeman, H. A., and Van de Steeg, J. A. (2010).
I. (2019). The house cricket (Acheta domesticus) as a novel food: a risk Sustaining intensification of smallholder livestock systems in the tropics.
profile.
Livestock Sci. 130, 95–109. doi: 10.1016/j.livsci.2010.02.014
J. Insects Food Feed 5, 137–157. doi: 10.3920/JIFF2018.0021
Moffitt, C. M., and Cajas-Cano, L. (2014). Blue Growth: The 2014
Ghani, A., Ferguson, N., Donnelly, C., Hagenaars, T., and Anderson, R. (1998).
FAO state of world fisheries and Aquaculture. J. Fish. 39, 552–553.
Estimation of the number of people incubating variant CJD. Lancet 352,
doi: 10.1080/03632415.2014.966265
1353–1354.
Monsees, H., Kloas, W., and Wuertz, S. (2017). Decoupled systems on
Ghani, M., Cozzolino, C. A., Castelli, G., and Farris, S. (2016). An overview of the
trial: eliminating bottlenecks to improve aquaponic processes. PLoS ONE
intelligent packaging technologies in the food sector. Trends Food Sci.
12:e0183056. doi: 10.1371/journal.pone.0183056
Technol. 51, 1–11. doi: 10.1016/j.tifs.2016.02.008
Mourad, M. (2016). Recycling, recovering and preventing “food waste”:
Gill, O. N., Spencer, Y., Richard-Loendt, A., Kelly, C., Dabaghian, R., Boyes,
competing solutions for food systems sustainability in the United States
L., et al. (2013). Prevalent abnormal prion protein in human appendixes
and France. J. Clean. Prod. 126, 461–477. doi: 10.1016/j.jclepro.2016.
after bovine spongiform encephalopathy epizootic: large scale survey. BMJ
03.084
347:f5675. doi: 10.1136/bmj.f5675
National Food Agency (NFA) (2018). Kontroll av Restsubstanser i Levande Djur
Gounden, C., Irvine, J. M., Wood, R. J. (2015). Promoting food
och Animaliska Livsmedel (Results From the Swedish Monitoring of Residues
security through improved analytics. Procedia Eng. 107, 335–336.
in Animals and Animal Products in 2016). Uppsala: Livsmedelsverket. (in
doi: 10.1016/j.proeng.2015.06.089
Swedish with English summary) Available online at:
Graiver, D. A., Topliff, C. L., Kelling, C. L., and Bartelt-Hunt, S. L. (2009). Survival https://www.livsmedelsverket.se/
of the avian influenza virus (H6N2) after land disposal. Environ. Sci. Technol. globalassets/publikationsdatabas/rapporter/2018/restsubstanser-kontrollen-
43. 4063–4067. doi: 10.1021/es900370x 2016-livsmedelsverket-nr-6-2018.pdf (accessed July 9, 2019).
Helland, J., and Sörbö, G. M. (2014). Food Security and Social Conflict. CMI
Newsome, R., Balestrini, C. G., Baum, M. B., Corby, J., Fisher, W., Goodburn, K.,
Report 2014:1. Bergen: Christian Michelssen Institute.
et al. (2014). Applications and perceptions of date labeling of food. Compr.
Hennekinne, J. A., De Buyser, M. L., and Dragacci, S. (2012). Rev. Food Sci. Food Technol. 13, 744–769. doi: 10.1111/1541-4337.12086
Staphylococcus aureus and its food poisoning toxins: characterization
Nyberg, K., and Lindqvist, R. (2017). Tillväxt av Bakterier Under Avsvalning,
and outbreak investigation. FEMS Microbiol. Rev. 36, 815–836.
Förvaring och Upptining (Bacterial Growth During Cooling, Storage and
doi: 10.1111/j.1574-6976.2011.00311.x
Thawing). Livsmedelsverkets Rapportserie nr 2 del 2/2017. Uppsala: National
Jasovský, D., Littmann, J., Zorzet, A., and Cars, O. (2016). Antimicrobial Food Administration.
resistance-a threat to the world’s sustainable development. Ups. J. Med. Sci. 121,
Nychas, G. J. E., Panagou, E., and Mohareb, F. R. (2016). Novel approaches for
159–164. doi: 10.1080/03009734.2016.1195900
food safety management and communication. Curr. Opin. Food Sci. 12, 13–
Johnson, L. K., Dunning, R. K., Bloom, J. D., Gunter, C. C., Boyette, M. D., 20. doi: 10.1016/j.cofs.2016.06.005
and Creamer, N. G. (2018). Estimating on-farm food loss at the field level:
Oivanen, L., Mikkonen, T., and Sukura, A. (2000). An
a methodology and applied case study on a North Carolina farm. Resour.
outbreak of trichinellosis in farmed wild boar in Finland.
Conserv. Recy. 37, 243–250. doi: 10.1016/j.resconrec.2018.05.017
APMIS 108, 814–818. doi: 10.1111/j.1600-0463.2000.
Johnstone, S., and Mazo, J. (2011). Global Warming and the Arab Spring. J.
tb00003.x
Surviv.
Poyatos-Racinero, E., Ros-Lis, J. V., Vivancos, J. L., and Martinez-Manes,
53, 11–17. doi: 10.1080/00396338.2011.571006
R. (2018). Recent advances on intelligent packaging as tools to reduce
Jurgilevich, A., Birge, T., Kentala-Lehtonen, J., Korhonen-Kurki, K., Pietikäinen,
food waste. J. Clean. Prod. 172, 3398–3409. doi: 10.1016/j.jclepro.2017.
J., Saikku, L., et al. (2016). Transition towards circular economy in the food
11.075
system. Sustainability 8:69. doi: 10.3390/su8010069
Rockström, J., Williams, J., Daily, G., Noble, A., Matthews, N., Gordon, L., et al.
Lagerberg Fogelberg, C., Vågsholm, I., and Birgersson, A. (2011). Från Förlust Till
(2017). Sustainable intensification of agriculture for human prosperity and
Vinst - Såhär Minskar vi Matsvinnet i Butik. (In Swedish, English
global sustainability. Ambio 46, 4–17. doi: 10.1007/s13280-016-0793-6
summary). Available online at:
Rocourt, J., BenEmbarek, P., Toyofuku, H., and Schlundt, J. (2003). Quantitative
https://www.slu.se/globalassets/ew/org/inst/energy- technology/oldies/nj-
risk assessment of Listeria monocytogenes in ready-to-eat foods: the
energi-och-teknik/lagerbergfogelberg-vagsholm- birgersson-2011-fran-
FAO/WHO approach. FEMS Immunol. Med. Microbiol. 35, 263–267.
forlust-till-vinst---sahar-minskar-vi-matsvinnet-i- butik.pdf (accessed July
doi: 10.1016/S0928-8244(02)00468-6
5, 2019).
Ropodi, A. I., Panagou, E. Z., and Nychas, G. J. E. (2016). Data mining
Lebersorger, S., and Schneider, F. (2014). Food loss rates at the food retail,
derived from food analyses using non-invasive/non-destructive analytical
influencing factors and reasons as a basis for waste prevention measures. Waste
techniques; determination of food authenticity, quality & safety in tandem
Manag. 34, 1911–1919. doi: 10.1016/j.wasman.2014.06.013
with computer science disciplines. Trends Food Sci. Technol. 50, 11–25.
Leibler, J. H., Dalton, K., Pekosz, A., Gray, G. C., and Silbergeld, E. K.
doi: 10.1016/j.tifs.2016.01.011
(2017). Epizootics in industrial livestock production: preventable gaps
Salemdeeb, R., zu Ermgassen, E. K., Kim, M. H., Balmford, A., and Al-Tabbaa, A.
in biosecurity and biocontainment. Zoonoses Public Health 64, 137–145.
(2017). Environmental and health impacts of using food waste as animal
doi: 10.1111/zph.12292
feed: a comparative analysis of food waste management options. J. Clean.
Lindqvist, R. (2019). L 2019 nr 02: Sjukdomsbördan av Inhemska Fall av
Prod. 140, 871–880. doi: 10.1016/j.jclepro.2016.05.049
Matförgiftning (Disease Burden for Domestically Aquired Cases of Food
Salman, M., Silano, V., Heim, D., Kreysa, J. (2012). Geographical
Borne Diseases). Livsmedelsverkets Rapportserie. Uppsala. In Swedish with
BSE risk assessment and its impact on disease detection and
English summary Available online at: https://www.livsmedelsverket.se/
dissemination. Prev.Vet. Med. 105, 255–264. doi: 10.1016/j.prevetmed.2012.
bestall-ladda-ner-material/sok-publikationer/artiklar/2019/l-2019-nr-02-
01.006
sjukdomsbordan-av-inhemska-fall-av-matforgiftning-smittskyddsunderlag-
Schneider, F. (2013). The evolution of food donation with respect to waste
del-1-livsmedelsverkets-rapportserie (accessed July 4, 2019).
prevention. Waste Manag. 33, 755–763. doi: 10.1016/j.wasman.2012.10.025
Lipinski, B., Hanson, C., Lomax, J., Kitinoja, L., Waite, R., and Searchinger,
Smith, M. D., Roheim, C. A., Crowder, L. B., Halpern, B. S., Turnipseed, M.,
T. (2013). Reducing Food Loss and Waste. Working Paper, Installment 2
Anderson, J. L., et al. (2010). Economics. Sustainability global seafood. Science
of Creating a Sustainable Food Future. Washington, DC: World Resources
327, 784–786. doi: 10.1126/science.1185345
Institute. Available online at: http://www.worldresourcesreport.org (accessed
March 1, 2019).
Lovins, A. B. (1990). The Negawatt revolution. Across Board 27, 21–22.
Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16
Vågsholm et Food Security, Safety, Sustainability Trade-Offs

SOU (2007). Betankandet om Jordbruket som Bioenergiproducent (Report on WHO (2015). Global Action Plan on Antimicrobial Resistance. Geneva: World
Agriculture as Supplier of Bioenergy). (In Swedish). Available online at: Health Organization. Available online at: https://apps.who.int/iris/bitstream/
http:// www.regeringen.se/sb/d/8963/a/81974 (accessed Jan 16, 2020). handle/10665/193736/9789241509763_eng.pdf?sequence=1 (accessed Oct 14,
Sundström, J. F., Albihn, A., Boqvist, S., Ljungvall, K., Marstorp, 2019).
H., Martiin, C., et al. (2014). Future threats to agricultural food Wilesmith, J. W., Wells, G. A., Cranwell, M. P., and Ryan, J. B. (1988).
production posed by environmental degradation, climate change, and Bovine spongiform encephalopathy: epidemiological studies. Vet. Rec.
animal and plant diseases – a risk analysis in three economic and 123, 638–644.
climate settings. Food Secur. 6, 201–215. doi: 10.1007/s12571-014- 0331- Willett, W., Rockström, J., Loken, B., Springmann, M., Lang, T., Vermeulen,
y S., et al. (2019). Food in the Anthropocene: the EAT-Lancet Commission
Swedres-Svarm (2018). Consumption of Antibiotics and Occurrence of Antibiotic on healthy diets from sustainable food systems. Lancet 393, 447–492.
Resistance in Sweden Solna. Uppsala: Public Health Agency of Sweden and doi: 10.1016/S0140-6736(18)31788-4
National Veterinary Institute. Wooldridge, M., Hartnett, E., Cox, A., and Seaman, M. (2006). Quantitative risk
Tabatabaei, M., Karimi, K., Kumar, R., and Horváth, I. S. (2015). Renewable assessment case study: smuggled meats as disease vectors. Rev. Sci. Tech. 25,
energy and alternative fuel technologies. Biomed Res. Int. 2015:245935. 105–117. doi: 10.20506/rst.25.1.1651
doi: 10.1155/2015/245935
The inquiry into BSE and Variant CJD of the United Kingdom (2002). Available
Conflict of Interest: The authors declare that the research was conducted in the
online at: http://webarchive.nationalarchives.gov.uk/20090505194948/http://
absence of any commercial or financial relationships that could be construed as
www.bseinquiry.gov.uk/ (accessed July 10, 2019).
a potential conflict of interest.
Unaegbu, EU and Baker, K. (2019). “Assessing the potential for energy from
waste plants to tackle energy poverty and earn carbon credits for Nigeria”.
The reviewer RK-T and handling editor declared their shared affiliation at
Int. J. Energy Policy Manag. 4, 8–16.
the time of the review.
Unilever Reducing food loss and waste (2019). Available online at: https://www.
unilever.com/sustainable-living/reducing-environmental-impact/waste-and-
Copyright © 2020 Vågsholm, Arzoomand and Boqvist. This is an open-access article
packaging/reducing-food-loss-and-waste/ (accessed March 1, 2019).
distributed under the terms of the Creative Commons Attribution License (CC BY).
United Nations (2019). Revision of World Population Prospects. Available online at:
The use, distribution or reproduction in other forums is permitted, provided the
https://population.un.org/wpp/ (accessed June 26, 2019).
original author(s) and the copyright owner(s) are credited and that the original
Vidaver, A. K. (2002). Uses of antimicrobials in plant agriculture.
publication in this journal is cited, in accordance with accepted academic
practice.
Clin. Infect. Dis. 34(Suppl. 3), S107–10. doi: 10.1086/ No use, distribution or reproduction is permitted which does not comply with
these
340247 terms.

Frontiers in Sustainable Food Systems | www.frontiersin.org 1 February 2020 | Volume 4 | Article 16

You might also like