Seguridad Alimentaria Algunas Tendencias Globales
Seguridad Alimentaria Algunas Tendencias Globales
Seguridad Alimentaria Algunas Tendencias Globales
com/myfreefoodindustry
https://www.facebook.com/myfreefoodindustrybooks/
We are IntechOpen,
the world’s leading publisher of
Open Access books
Built by scientists, for scientists
4,000
Open access books available
116,000
International authors and editors
120M Downloads
154
Countries delivered to
TOP 1%
most cited scientists
12.2%
Contributors from top 500 universities
Chapter 1
Yehia El-Samragy
Yehia El-Samragy
Additional information is available at the end of the chapter
Additional information is available at the end of the chapter
http://dx.doi.org/10.5772/intechopen.79131
1. Introduction
On a global scale, there has been a notable elevation in the extent of foodborne diseases,
in addition to disturbances in the international food trade resulting from recurrent disputes
with regards to food safety requirements. In order for improvements to be recognized in
food safety systems, most of these systems need to be reviewed and further developed. It is
especially crucial at the present time, for both developed and developing countries, to create
and propagate food safety systems in accordance with the principals of risk-based thinking
and risk assessment. Therefore, it is important to be equipped with important knowledge on
the principles and practices of food safety systems and the trend that will take food processors
away from a merely reactive approach to food safety procedures, to a more proactive one.
The responsibility of the control of food safety worldwide is shared between several different
agencies and ministries of the same country. The roles and responsibilities of these bodies may
be quite different but most of the time can be considered as a kind of duplication of the same
regulatory activity where unnecessary routine inspection visits and a lack of coordination are
common. Moreover, the expertise and resources of these different agencies are varied, which
can create a conflict between the responsibilities for protecting public health and obligations
toward either facilitating trade or developing an industry or a sector.
© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons
© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative
Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
distribution, and reproduction in any medium, provided the original work is properly cited.
https://www.facebook.com/myfreefoodindustrybooks/
involved in the management and control of food safety has become the utmost importance.
The importance of developing effective relationships and mutual support among government
agencies and institutions involved in the control of food safety and other interested parties,
particularly the food industry and consumer associations, will enhance the establishment of
effective food safety systems that positively impact the public health.
Since 1990s, food safety systems and code of practices have been developed substantially.
These developments have been driven primarily by the implementation of the Hazard
Analysis and Critical Control Point (HACCP) system for ensuring food safety worldwide,
as well as compliance with International Organization for Standardization (ISO)-issued stan-
dards by different sectors of the food industry, including but not limited to the food chain.
As a result, it has now become a necessity for students being prepared to start their career
paths in the food industry to become educated about these safety systems, while still in their
undergraduate programs.
The most important method for protecting public health is by promoting food safety that
has long been recognized as a governmental responsibility in any country. It has improved
through a series of statutory and regulatory requirements that responded to the fact that a sig-
nificant proportion of human illnesses and deaths often have their origin in the food supply.
Most of the food safety studies were to place emphasis on microbiological criteria used
currently in the different food commodities, as the issues surrounding food safety criteria
are common to all sectors of the food chain. The observation of foodborne disease and the
monitoring of microbial contaminants of food, both from a public health standpoint and con-
trol measures of the effectiveness of food safety criteria must be practiced. The suggested
science-based strategy for developing food safety criteria, including the standard operating
procedures and instructions for their implementation, should be described for obtaining the
best data to support this process.
Therefore, the scope of each study should cover these food safety criteria and should work to
evaluate the scientific basis for existing microbiological criteria applicable to the selected food
sectors, in addition to the extent to which these standards are suitable tools of ensuring the
safety of such foods within any food safety systems based on the Hazard Analysis and Critical
Control Point System (HACCP). The scope should follow the science-based process to set up
food safety criteria and recommend guidelines as to what data are adequate and appropriate
for use in developing new, or improving current criteria. The extent of the study should exam-
ine whether current criteria fulfill what they are required to achieve and the need to connect
science-based criteria to public health objectives. Revision of the need for performance stan-
dards as control measures of food safety hazards and the way such criteria are implemented
within HACCP system should take place to the extent that ensures processing of safe food.
The recommended amendments for continual improvement should take into consideration
the requirements of all the interested parties, i.e., consumer, industry, and food legislators.
https://www.facebook.com/myfreefoodindustrybooks/
Moreover, the availability of different food safety standards to agencies in charge of regula-
tion should be oriented toward creating a connection between performance indicators and not
only public health targets but also the economical aspects of food safety criteria, in addition to
providing recommendations for continual development. This can be done via implementation
and subsequent development of science-based criteria for food safety; criteria that include
principals for managing the degree of risk for foodborne illnesses and becoming familiar with
the elements that contribute to that risk.
The safety of our food products must always be given top priority in all that we do through
selecting the best standards for an operation and then defining, implementing, maintaining,
and continuously improving the food safety system. It is very important along all the steps
of this process that food professionals monitor the specific sources related to the standard of
choice along with staying up-to-date on current food safety-related news and incidents.
Author details
Yehia El-Samragy
Address all correspondence to: elsamragy@hotmail.com
Food Science Department, Faculty of Agriculture, Ain Shams University, Cairo, Egypt
https://www.facebook.com/myfreefoodindustrybooks/
Chapter 2
http://dx.doi.org/10.5772/intechopen.73687
Abstract
Food safety is a complex topic, and the various market participants are involved, such as
authorities, non-governmental organisations (NGOs), consumer protection bodies and the
media, have a very different, often emotionally charged perspective. This poses a particu-
lar challenge to producers and distributors when deciding on a method to deal with
media attention on unhealthy food, with contaminations and residuals. There are numer-
ous examples of crises caused by impermissible residuals. This shall be illustrated using
concrete examples from the egg, game and poultry industries.
Keywords: basics food law, health risks, microbiological dangers, residuals, HACCP
concept, standards, crisis management, preventions
1. Introduction
Food safety is paramount in the food chains with raw materials contaminations, improper
treatment or storage and incorrect declarations or expiration dates having become a daily
occurrence. Almost every German food company, as well as food companies in other countries,
experiences at least one so-called food crisis over the course of its activities. These are often
triggered by inconspicuous events that are not indicative of a threat initially. However, experi-
ence has shown that what seems like harmless negative customer feedback or complaints can
give rise to a full-blown crisis. The consequences are often initiated by media warnings, which
might in turn lead to product recalls. These are subsequently published by the supervisory
authorities in the European Rapid Alert System for Food and Feed—RASFF [1]. This is associ-
ated with high costs and time expenditures for those parties involved. As a result, recalls can
even threaten the very existence of the distributing company responsible. Moreover, the distri-
bution of unsafe food is usually associated with significant image loss. At the same time, the
question arises when food should be considered hazardous to health following the legal
© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
https://www.facebook.com/myfreefoodindustrybooks/
intention of the general administrative regulations of the EU Rapid Alert System. The Article
Food Safety and Crisis Management illustrates this using several real practical examples,
which the author Caspar von der Crone has overseen as responsible manager [2] over the
last years.
The general rule is: Food that is not safe may not be distributed. This is regulated by EU
Regulation (EC) No. 178/2002 (Basic Regulation) [3]. In addition, national regulations apply
as for example the German Food and Commodities Act (LFGB) [4]. In a European Law
framework, food is only considered unsafe if it can be assumed that it is harmful to health. In
addition, food is also considered unsafe if it can be assumed that it is not suitable for human
consumption. A differentiation is in order here, as the first description is concerned with
defending against health risks, while the second description only serves to secure commercial
consumer interests. Put differently, consumers’ commercial interests—and not their physical
integrity—should be protected from bad buys and unpleasant surprises to the greatest possi-
ble extent.
The objective is a sustainable business condition along the entire process chain, as shown in
Figure 1 (overview), under the inclusion of ecological, economical and social aspects. This
applies in equal measure to the entire value-added chain, under the consideration of the
respective process steps, starting at the producer and ending at the consumer. The legal
requirements must be included, as well as the interests and requirements of NGOs, paying
particular attention to consumer’s expectations, who make the decision in the end and are an
important part of the process chain.
3. Control scenarios
Modern food control, in other words, is the control for ‘means of live’ [5]. Figure 2 is still at a
nascent stage; however, its roots date back far into the past. Controls to ensure that consumer
demands for healthy food were met have been in place for ages. German Food Law’s history
can be traced to the Middle Ages. Here, the objectives were to fight wine adulterating or
counteract the growing public health risk posed by raw materials that are hazardous for
health, among others. Regulations for meat production were introduced at a very early stage,
with relevant hygiene directives. Regulations concerning the restructuring of food contact
materials (LMBG) were introduced in the 1970s, which allowed the state to act to protect
consumers against damage to health.
The survey conducted by the European Commission in their White Paper on Food Safety from
2000 is additionally worth mentioning. In it, the Commission worked out a division of food
safety responsibilities between the involved actors, with the main responsibility for food safety
lying with the feed producers, the farmers and the food producing companies. In this context,
the HACCP concept (Hazard Analysis and Critical Control Point) was introduced, which
obligates the food company operators to danger analyses and conceptual assessments. The
FAO/WHO Codex Alimentarius offers an internationally binding version, which in turn is part
of the ‘General Principles of Food Hygiene’. With the HACCP concept, health risks posed by
food should be identified, evaluated and managed.
4. Monitor CCPs.
https://www.facebook.com/myfreefoodindustrybooks/
5. Establish corrective action. These shall be implemented if monitoring shows that a certain
CCP is no longer under control.
6. Preparing procedures to verify and confirm the successful operation of the HACCP system.
7. Recordkeeping that considers all processes and records concerning the principles and their
application.
With the EU Basic Food Regulation, the European Food Safety Authority (EFSA) was
established. The EFSA assumes tasks that relate to the scientific evaluation of relevant food
topics at the EU level. The EFSA is also the point of contact for the scientific evaluations related
to certain approval procedures, for example during the approval of food additives.
Every food producer is subject to controls along the entire process chain, starting at the farmer/
producer up to the food retailer, to inspect the adherence to relevant production standards.
Over the last years, many standard-setting bodies have established themselves on the market.
In the area of egg production, this is the KAT System (Association for Controlled Alternative
Animal Husbandry) [6]; for meat production, the QS GmbH (Quality scheme for food) [7].
Both systems cover the entire process chain with specific standards and criteria, and they are
ultimately demanded by retailers for animal product distribution. The International Featured
Standard (IFS) [8] is another controlling body, a standard developed by the food retailers that
places very stringent process quality and traceability demands on processing companies. The
IFS Standard offers additional safety guarantees. The controls take place annually, with the so-
called integrity audits (unannounced inspections) offering further security. By now, producers
and distributors from across the globe operate by the IFS Standard to meet globalised quality,
transparency and efficiency demands. It ensures that the certified companies attain a high
quality and product safety standard.
Figure 1 represents the dialogue between scientific and regulatory actors within the process chain.
Biological, chemical and physical agents, as well as insufficient allergenic property informa-
tion, can all pose health hazards. Additionally, the German General Administrative Regulation
for the implementation of the Rapid Alert System for Food, Food Contact Material and Feed
(AVV Schnellwarnsystem) [9] offers a guideline for the evaluation of a food that poses a poten-
tial health hazard. However, it should be noted that the General Administrative Regulation
has no legally binding qualities and solely serves to harmonise the implementation of Food
Law. Put differently, the General Administrative Regulation has an internally binding effect for
the Food Enforcement Authority at most.
The normal consumer usage conditions should first be considered when deciding whether a
food product is safe or not. For example, this relates to improper handling, which runs counter
to the principle of proper kitchen hygiene in a private residence such as improper storage of
products that should be refrigerated.
The result is that hazardous food products purchased by consumers should be recalled pub-
licly via the media, while the product that is ‘only’ unsuitable for human consumption will be
recalled ‘quietly’ through the commercial buyers.
https://www.facebook.com/myfreefoodindustrybooks/
Biological, chemical and physical agents, as well as insufficient information about allergenic
properties, can pose particularly significant consumer health hazards. The normal consumer usage
conditions should first be considered at all levels when deciding whether a food product is safe or
not. This means that those types of usage which are not normal but at the same time imaginable
should also not lead to situations that might be hazardous. However, improper handling after
purchasing, insufficient adherence to hygienic principles in private residences, incorrect storage of
products that should be stored under refrigerated conditions, or also the consumption of raw
poultry might have negative health effects and lead to illness. Even if this lies outside the distrib-
utor’s scope of responsibilities, it might be hard to interpret evidence pertaining hereto.
The high incidence of salmonella in the beginning of the 1990s is a good example of this. The
illness was primarily caused by the consumption of eggs or egg products (tiramisu and other
dishes containing raw eggs). Even though the root cause was improper handling and failure to
adhere to refrigeration guidelines, eggs were still suspected to be highly pathogenic, which
subsequently led to a significant consumption reduction. German legislators reacted with
national cooling regulations from the 18th day onwards. This regulation was only lifted a few
years ago, when it is known that cause and effect had been mixed up. There are still salmonellae;
however, consumer education through advice on egg storage after purchase, as well as consis-
tent salmonellae monitoring at the production level, led to a greater degree of food safety. The
same problems have not occurred, even though the regulation prescribing cooling from the 18th
day onwards has been lifted.
This serves to illustrate that a decision on a food product’s safety should also consider that
information communicated to the consumer—including label information and cooking recom-
mendations—contributes to safety. The packaging advice ‘heat before consumption’ is another
classic example that helps avoid health hazards; this instruction points out to the consumer
that the food should be treated accordingly, that is to say, not consumed raw.
This particularly applies to raw poultry meat, for the lion’s share of relevant germs is killed if
these products are heated at 70 C for at least 10 min. This also includes good kitchen hygiene
and know-how on handling and processing food intended for immediate consumption.
The exact definition of a hazard to human health as it relates to regulations is not concretised
or clarified further legally. However, as it concerns a hazard that is triggered by the consump-
tion of affected food, the basics of Food Law apply at the least. Following Article 3 (14) of the
Basic Regulation, a hazard is a biological, chemical or physical agent in a foodstuff, or condi-
tion of a foodstuff, that might negatively influence health.
In principle, physical, biological and chemical hazards to human health are imaginable. How-
ever, in the production of food commodities, focus is clearly placed on ‘chemical components’
due to the complex structures [10].
https://www.facebook.com/myfreefoodindustrybooks/
Biological dangers that originate from the commodity itself are not plausible. If finished
products, such as kitchen utensils, are passed onto the consumer, there is only limited neces-
sity due to the common household cleaning before use.
The circumstances are different for convenience food. A possible, if still unlikely, practical
scenario might be the contamination of food commodities during production, for example
due to an ill employee. Today, legal requirements (instruction obligations) make the risk of
transmitting certain legally relevant illnesses significantly less likely and rather negligible.
Food commodities can also pose a threat through physical contamination. Foreign bodies, as well,
are not that uncommon. Material fatigue and damages might lead to foreign bodies entering a
food product such as metal residues because of a malfunctioning or broken metal detector.
Another example comes from game: metal residues from pellets have led to a (in part com-
plete) ban on wild hare meat. However, this was not due to the metal residues themselves, but
rather due to the fact that the pellets contained lead. Lead residues in game can pose a risk to
human health from a food inspection perspective. Pellets containing lead were the standard
hunting shot until recently. The German Federal Ministry of Food and Agriculture (BMEL)
[11], German Federal Institute for Risk Assessment (BfR) [12] and the European Poultry, Egg
and Game Association (EPEGA) [13] have assumed responsibility and performed large-scale
lead-residual monitoring in killed game. The research project ‘Food Safety of Killed Game’ can
be accessed publicly on the BMEL website.
The results did not indicate a direct health hazard with proper hunting. However, the indi-
cated consumption was rather negligible at 0.5 kg per inhabitant. All the same, heavy game
consumers (hunters), children and pregnant women were deemed at risk. The situation has led
to changes as lead-containing shot is increasingly replaced by lead-free ammunition since then.
This makes game a safe product again. This example shows that small effects can lead to
serious issues that cast shadows over entire industries.
5. Microbiological hazards
Food hazards are most commonly caused by microbiological organisms. Generally speaking,
bacteria play a vital role in food production. Useful bacteria influence food properties posi-
tively, think of aromas. Unwanted bacteria in and on food can negatively influence product
quality as spoilage agents or even pose a food safety risk as pathogenic agents.
Many food products—of animal origin in particular—present an ideal culture medium for
bacteria, offering optimal living and multiplication conditions. A classic example is the salmo-
nellae in the products containing raw egg or raw poultry mentioned before. Good hygiene is
essential in impeding the multiplication and spread of microorganisms. This also includes the
systematic cooling of food products of animal origin, which additionally stops the spreading of
germs. This makes compliance with the cooling chain another important preventative mea-
sure, just like proper heating.
The Commission Regulation (EC) No. 2073/2005 [14] on microbiological criteria for foodstuffs
offers a legal foundation. This regulation contains the so-called hygiene package from 2004,
https://www.facebook.com/myfreefoodindustrybooks/
with it, the European Union renewed its food hygiene regulations. Since 2004, there has been
another paradigm shift in the distribution of food product of animal origin. Another example
from the commercial exploitation of game: This industry was also plagued by complaints and
scandals that cast a shadow on the commercial viability of game distribution, as old traditions
were followed, and the cooling chain was not immediately adhered to, or adhered to at all,
after the kill. This led to microbiological values that in part far exceeded the regulated maxi-
mum values and in turn led to recalls and closures of game-processing companies. In his
function as the General Manager of European Poultry, Egg and Game Association, the author
of this article initiated regulations for good game hygiene, connected to a microbiological
assessment. This was in the interest of the associations’ member companies and served as a
foundation for consumer health protection. Extensive studies of killed game under various
cooling requirements and game carcase treatment after killing showed that it is well possible to
adhere to the microbiological regulations. The so-called game guidelines [15], with specific
provision for the handling of killed game and distribution regulations, as well as the associated
consequences, have established standards that ultimately contributed to restoring consumer
trust, making properly treated game considered a safe food product again.
The illustrations and explanations on food safety mentioned above merely represent a foray
into Food Law. The regulations are very complex at a national and EU level and cannot be
treated more comprehensively in this article. In the following discussion of food safety, further
practical examples serve to illustrate the influence of crisis management and food safety.
All parties involved in refining food products, at all levels, are responsible for their safety, with
the primary responsibility placed on the producer. The responsibilities of producers and
distributors are orientated following the principle of concrete influences within the scope of
activities. Additionally, the producers should, in the context of their business activities, take all
measures appropriate to recognise potential hazards, befitting the properties of the products
they deliver, and to take precautions against potential consumer hazards.
Figure 3 illustrates the various process levels. Here, each participant bears equal responsibility
for the safety of a certain product, from production to the final customer purchase. The parties
involved should assure that the condition and labelling of the product adhere to all legal
requirements along the entire chain. The requirements that apply at the various process levels
are provided by the government, while nongovernmental organisations significantly influence
the public opinion formation process during crises. A constructive dialogue with the supply
chain should take place with the relevant stakeholders.
7. Crisis management
Crisis management above all entails crisis management in collaboration with the responsible
authorities. Attempts by a company to cover up or ignore an issue are particularly problematic.
The author of this article has faced numerous crises up front, providing the practical experience
to manage these. In the following, practical crisis examples are used to illustrate and elucidate
what measures can be used in what ways to guarantee a future-proof presentation of prevention.
Some essential perspectives on crisis management:
Customer, authority, or consumer complaints cannot be left unanswered. They are a vital
source of information about the safety of a company’s products. In principle, it does not matter
whether a customer complains that a product expired before the indicated expiry date, or that
this is documented in an officially logged complaint. In all cases, the same concrete circum-
stance applies, namely, that the products expired before the expiry date. This might have
various causes, some of which might not be attributable to the producer (for example, an
interruption of the cooling chain at the retailer).
If the food business operator fails to follow up on this complaint and fails to process this
complaint in an appropriate manner, the situation might develop into an actual crisis. This
rings true particularly considering the fact that authorities, after repeat comparable violations,
no longer assume negligence but rather accuse the food business operator of intent.
Within a crisis management context, all procedures and work instructions relating to the
handling process of complaints should be defined. An example of this is the development of
forms for consumer complaints to help employees summarise complaints by phone or in
writing, with an accompanying work instruction. Here, the development of a crisis plan is of
the utmost importance, and this is a type of work instruction that prescribes how to act in crisis
situations. This not only applies to the company itself; authorities are also obligated to develop
crisis plans. This is fundamentally regulated by the Basic Regulation of the European Com-
mission, which drafts a general crisis management strategy together with the European Food
Safety Authority (EFSA) and the member states. This strategy is used if the preventive, curative,
and reductive risk measures defined in the Basic Regulation do not suffice.
https://www.facebook.com/myfreefoodindustrybooks/
Another method to improve food safety lies in informing consumers, by increasing their
knowledge of food and certain potential hazards related to food. Poultry offers another exam-
ple. If it is cleaned in water that is subsequently used to wash lettuce leaves, this might lead to
salmonellae finding their way into the food. This is why good kitchen hygiene practices are of
cardinal importance. Gaps in consumer knowledge can be filled by relevant product informa-
tion or by informational campaigns. This information should be written in simple language.
This goes to show that ‘risk minimisation’ is a very diverse topic, some practical examples are
explored in the following.
The so-called dioxin crisis at the end of 2011 led to an official warning about foodstuff that was
not suitable for distribution. This crisis primarily affected eggs and poultry. Noteworthy about
this crisis is not the circumstance that fatty acids in milk which might contain dioxins—
primarily intended for technical purposes—were potentially mixed in with compound feed
for animal rearing in a feed plant. The actual cause was dioxins in this feed that stored
themselves in the fatty acid, leading to egg and poultry meat contamination, among other
animal product contaminations, later.
Dioxins have led to significant problems in the past. The first of these was a chemical accident
in Seveso, Italy, in the middle of the 1970s, with approx. 2 kg of dioxins released into the
environment, leading to serious diseases. Dioxin is considered a carcinogen with significant
adverse health effects, which in turn explains the fears of consumers, as well as the potential
effects of dioxin residues.
The Belgian dioxin crisis took place in 1999. The improper use of frying oils in animal feed led
to dioxin findings in eggs. At the time, this had catastrophic effects on egg consumption, which
was virtually reduced to zero out of fear for diseases. The emotional perception played an
enormous role in this, even though only relatively minor dioxin traces were found. However,
the actual problem was that the egg origins could not be traced, which led to all eggs being
taken off of retailers’ shelves.
As a consequence, the Association for Controlled Alternative Animal Husbandry (KAT), at the
time headed by Caspar von der Crone, advocated a general ban on feed with animal protein.
While this might increase production costs, it would allow the industry to regain consumer
trust, capable of contributing significantly to food safety.
Another case occurred in 2002, the so-called Nitrofen scandal. Nitrofen is an herbicide that had
been used in the agricultural industry. It turned out later that Nitrofen is a carcinogen that is
not broken down by the body but rather stored in animal fatty tissue, which can in turn be
found in the eggs of laying hens. These residuals were found in the summer of 2002. Nitrofen
was one of many pesticides already forbidden in the EG but still allowed in the DDR up to
1999. This led to remaining stock with contaminated feed in a storage after the German
reunification, which was in turn inspected and cleaned insufficiently before being fed to laying
hens as organic feed, among others.
https://www.facebook.com/myfreefoodindustrybooks/
This gave rise to another scandal, in the area of organic production, with extensive recall
actions as a result. The affected companies could be identified exactly in the beginning. The
database system developed by KAT at the time, striving to safeguard traceability, as well as the
newly introduced identification measures for individual eggs with origin labelling, proved to
be an effective preventative measure. For the first time, it was possible to recall contaminated
eggs in a targeted manner, avoiding any negative effects or harm to consumers.
The affected companies suffered significant losses, even threatening their very existence, but
managed to rebuild trust through consistent action-taking. There was an awareness that
product traceability is one of the most important food safety criteria in crisis situations. This
led to the EC decision to adopt individual egg labelling as a binding requirement for egg
distributors across the EU.
The dioxin crisis of 2011 took place under similar circumstances. Affected companies were
closed, and recall actions were initiated. Media pressure was enormous, and consumers were
requested to either return or destroy food, primarily eggs and poultry. Thanks to KAT and
the mandatory producer code printed on each egg [16], the eggs origins could be traced. The
names of the affected companies—publicly traceable through the code—were disclosed by
authorities with an accompanying warning. However, the eggs already reached consumers’
refrigerators, as the dioxin was discovered in November, but the authorities did not inform
consumers of dioxin residue hazards until January 2012. At this point, most eggs were
already consumed. Similar recall actions were initiated for poultry; however, this proved to
be significantly more difficult as poultry was not distributed using the same traceability
system as the KAT individual egg labelling system. This led to immense reputation damage,
as well as more critical consumer attitudes, and in turn reduced egg consumption. Interest-
ingly, the organic food industry benefited from this, as consumers expected that the organic
industry adhered to stronger regulations and was subject to more stringent controls, improv-
ing safety.
At the end of 2014, the organic food industry was rattled by several events. Residues of a
corrosive agent and a fungal toxin were discovered, and the products of numerous companies
were stripped of the right to be sold with an organic seal as a result. The contaminated feed,
still labelled as ‘organic’ by a Dutch distributor, had been distributed to organic farmers in
Germany.
A total of 2000 tonnes of affected feed, sunflower cake, was distributed by a Dutch distributor
as organic feed. Organically producing laying hen companies, as well as pig, cattle and sheep
farmers, were affected.
There are no special restrictions for pesticide in place in conventional farming, quite different
from organic production, which uses stricter standards. The affected companies faced grave
consequences. Goods that had already been delivered were recalled by regional authorities,
and goods that were being produced currently could not be distributed for a certain period. It
is interesting to note that these regulations were only implemented in individual German
states, while the remaining lion’s share of cakes contaminated with pesticides could still be
processed for organic production in other EU countries. There was no health hazard, but rather
a component in the feed that is not permitted in organic production.
https://www.facebook.com/myfreefoodindustrybooks/
Regional German authorities, in the meantime, considered this circumstance consumer decep-
tion following the EU Regulation on Organic Farming [17], as this stipulates that only
uncontaminated organic feed can be used.
The most recent incident took place in the Netherlands in 2017, where the banned insecticide
(against mites) Fipronil was used. Again, contaminated eggs reached the market—almost
exclusively eggs produced in the Netherlands—which resulted in a recall for eggs with the
NL (the Netherlands) identification. Egg products were also affected, as were processed prod-
ucts such as cakes, noodles and other products containing egg. Here too, the individual egg
identification system proved very effective, with targeted recall measures, allowing for the
continued distribution of uncontaminated goods. However, processed products remained in a
grey area.
9. Preventative measures
Crisis situations can occur suddenly and unexpectedly, even in a carefully managed company.
Internal business process problems as well as external, unforeseen difficulties might be the
cause. Therefore, a preventative strategy should consider all potential measures that might
equip a company to deal with such situations.
This includes general preventative measures (quality measures, self-controlling systems fol-
lowing the HACCP concept principles, traceability, claims and complaints, false management,
and the like). Additionally, specific measures should be considered such as the development of
a crisis plan and special measures for at-risk products.
Therefore, any properly managed company requires a quality management book, in which the
procedural instructions regarding quality politics, as well as the principles of quality assur-
ance, are defined. By now, also in the light of increasing pressure of retailers, systems following
the International Feature Standard (IFS) have established themselves. This includes the British
Retail Consortium (BRC) [18] and Global Standard for Food Safety, with similar regulations.
A vital component of a quality management system is the aforementioned HACCP concept,
which is required following Art. 5 of the Regulation 852/2002 (EC) No. 852/2004 on Food
Hygiene. This regulation prescribes that food business operators must develop, implement
and maintain one or more procedures based on the HACCP principles.
10. Summary
Food safety is a very complex topic. Crises have repeatedly led to product recalls in the past
and significantly contributed to consumer unrest. This not only influenced consumption,
which collapsed in part, but also resulted in significant damage to the reputation of the
product itself. The examples mentioned from the egg, poultry and game industries illustrate
this very clearly. Minor triggers have shown time, and again that a critical light was cast on
many food products, also clean food products. Dioxins on forbidden ingredients can be
https://www.facebook.com/myfreefoodindustrybooks/
considered criminal. Environmental residues or soil contaminations, on the other hand, are
difficult to assess for producers and pose a risk that is hard to perceive. Oftentimes, these
findings are caused by so-called inherited contaminations, as can be seen in the organic egg
industry during the Nitrofuran crisis. Producers cannot be held accountable for this; however,
they do bear the full risk and consequences associated with this. Unfortunately, it has shown
repeatedly in the past that economic factors alone led to crises. The initial use of cheap
additives and other ingredients, which did not appear to contain contaminations but did in
the end, have contributed to this. Therefore, the food producer should be aware of the respon-
sibilities associated to these activities. However, it can certainly be recommended to inspect
purchased feed and similar products before use. Suppliers should have a certain certification.
Product recalls by authorities and public disclosure, as well as rapid alert systems (EC), are
further sensible measures. However, prevention is better than cure, and high-quality produc-
tion, as well as adherence to stringent standards, is paramount.
Acknowledgements
The author likes to thank Dr. Markus Grube, RA KWG, Gummersbach for his support and
critical reading of the manuscript.
Author details
References
[2] von der Crone, Managing Director KAT. Verein für kontrollierte alternative. Germany:
Tierhaltungsformen e.V. http://www.kat.ec
[3] EUR-LEX, website: http://eur-lex.europa.eu/legal-content/DE/TXT/?uri=celex:32002R0178
[4] JURIS, website: https://www.gesetze-im-internet.de/lfgb/BJNR261810005.html
Chapter 3
Additional
Additional information is available
information is available at
at the
the end
end of
of the
the chapter
chapter
http://dx.doi.org/10.5772/intechopen.75587
Abstract
1. Introduction
Food safety systems in developing countries are weak, fragmented, and not effective to pro-
tect consumer’s health or help countries competing for export markets. Improving food safety
often costs much (or is associated with additional costs which could only be recouped by the
items fetching more money) and many developed countries experience real challenge in mak-
ing food safety legislations work. At least, this is the perception of majority of SMEs. Many
years later after the unveiling of codex and ISO standards, these countries’ domestic markets
suffer from sustained food safety-related issues ranging from food-borne illnesses to food
© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons
© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative
Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
distribution, and reproduction in any medium, provided the original work is properly cited.
https://www.facebook.com/myfreefoodindustrybooks/
fraud. In spite of this, a lot of stride has been made with regard to development or adoption
of international standards; however, what remains to be seen is the full implementation and
hence marked decrease in food safety-related incidences [1].
Food safety concept continues to gain attention particularly in developing countries. Many
countries rely purely on small scale (subsistence) and street vendors to feed their popula-
tions. Yet, these traders are not usually included in the mainstream food safety systems.
In flow of substandard and poor quality goods, corruption, low income, unjust trade, and
political turmoil are ills deviling developing economies, and this adds to the challenge of
food safety systems’ operation. Generally, few of the developed countries have formalized
agriculture systems. To this extent, farm implements, fertilizers, seeds crop management
practices, and manufacturing are scattered across vast geographical locations. Food inse-
curity, political instability, outbreaks of communicable diseases and natural disasters are
challenges that compete for government attention; hence, food safety is often not prioritized.
Yet, the definition of food security from the 1996 World Food Summit Plan of Action men-
tions access to sufficient, safe, nutritious and affordable food to all people at all times. Often,
it seems that in developing countries, not enough emphasis is put on the safety aspect of
food security [2].
According to published data by FAO and WHO, about 2000 food-borne-related deaths occur
daily in Africa. Over 700,000 food-borne illnesses recorded annually are due to diarrheal-
related illnesses and from contaminated food and water. Salmonella, Shigella flexneri, Shigella
sonnei, Clostridium perfringens and other parasites are major culprits. An alarming average of
3.3–4.1 episodes of diarrheal diseases among children in Africa has also been recorded annu-
ally. Coupled with malaria, HIV, TB, these become more debilitating, creating a huge dent
on the public health’s integrity. Food-borne illnesses lead to reduced productivity, disability,
early deaths, low incomes and hence low access to food and the problem becomes cyclic.
Illegal use of food additives, (E110, E102, E104, and E124) in local and imported foodstuff
including infant foods, is an alarming case. Unless an approach that understands the unique
challenges of developing economies are employed, the great food safety legislations may
remain in revered books of codex without having a real impact on food safety situation in the
developing world [2].
First, developing countries bear the greatest global burden of food-borne illnesses and death.
The strain this adds to an already stretched public health services is huge. Second, regional
and international trade is becoming extremely invaluable. For this reason, more sensitivity
to food safety is needed. Benefits of safe, adequate, and nutritious food abound. It is crucial
to long-term economic growth, good health, and productivity. It is also associated with a
happier population that would enjoy reduced conflict. Countries in Africa and the rest of the
developing world have some form of legislation regarding food safety. Some of this, however,
https://www.facebook.com/myfreefoodindustrybooks/
are most rudimentary, archaic and at times not based on sound science. For these legisla-
tions to benefit the rest of the countries, there must be a push to align them to World Trade
Organization (WTO)’s agreement on the application of Sanitary and Phytosanitary (SPS) and
Technical Barriers to Trade (TBT) agreements and the Codex standards and codes of practice.
Some of the standards are not science-based as required by Codex in a bid to help facilitate
regional and international trade among different countries. This then curtails international
trade and sometimes creating a bad notion of standards among processors. Several factors
hamper the push to realize the implementation of food safety legislations in the countries
such as inadequate technical capacity, lack of awareness of economic loss arising from poor
quality foods, and weak enforcement of regulations among others [1]. The unveiling of the
ISO allowed for HACCP to be upgraded through the International Standard ISO22000:2005
(Food Safety Management Systems—Requirements for any organization in the food chain).
The ISO technical committee on food safety created in 1947 is one of ISO’s oldest and most
fruitful committees, with over 830 published regulations and 125 more in the pipeline. ISO
standards have played a crucial role in promoting global standards, development of har-
monization and awareness creation. In many developing countries, ISO 22000:2005 is not a
mandatory food safety requirement and perhaps due to its complexity, cost of compliance or
technicalities, only few companies that most of the times have qualified food safety experts
manage to get the certification.
2.1. Key food safety regulations at the world stage with an impact on developing
economies’ food safety
Africa has been reported to enjoy over 5% annual economic growth in the recent decade,
and this growth rate is predicted to continue or even improve in the next couple of years.
For African countries, opulence and affluence among her populace is creating a reason
for demand of high quality safe and mostly longer lasting products [2]. This can also be
said accurately of the rest of the developing economies especially in Asia as well as South
America. The Sanitary and Phytosanitary (SPS), World Trade Organization (WTO)’s—
Technical Barriers to Trade (TBT) agreements are some of the regulations that require atten-
tion of all countries involved in any trans-border trade particularly of agricultural produce.
The developing economies are huge exporters of raw or semi-processed agricultural goods,
and these put them directly under the requirements of these legislations. Though there exists
food safety standards in almost every country in one form or the other, these standards do
not adequately help to improve food safety because of two main reasons. First, imports
even of poor quality foods are not curtailed sometimes due to laxity, incapacity, or corrup-
tion. Some of the regulations are far stricter even beyond the codex requirements this more
often than not hinders trade especially inter-regional trade. Second, there is very low level
of implementation of regulations across board. This is why the regularization of laws and
their harmonization should come into play. There are few global organizations that are at
the forefront and with the expertise and neutrality to help countries navigate this concept of
global standards harmonization. One such initiative is the Global Harmonization Initiative
(GHI). More about the structure strategies and aims of the GHI and other such bodies are
discussed in a later subheading.
https://www.facebook.com/myfreefoodindustrybooks/
In general, it can be surmised that there are three major models adopted by countries in national
food control systems: the single agency model relies on one organization or umbrella body which
is mandated with all the functions of controlling food safety. This model has the advantage that
food safety issues are accorded priority, and they can be highly effective. The second model
implies multiple agency scenarios. In this case, the role of food safety is sector and commodity-
specific. In this system, the roles could also be devolved to federal, local governments or counties
and the national level. Some challenges with this model are: duplicity of functions, conflicts, and
differing expertise at national and at the regional level, reduced domestic consumer confidence
and confusion among stakeholders as to which laws to comply with. The third model is an inte-
grated system: in this system, agencies are assigned jurisdiction based on aspects of food safety
which cut across all the sectors such as policy development, coordination, inspection, education,
and training. Irrespective of the model that best suits a country, it must be based on the prin-
ciples of transparency, inclusiveness, integrity; clarity of roles, accountability, science/risk-based
approach and equivalence as the benchmarks against which its success is measured [3].
This gives the general direction and thrust to the food industry in a country and defines
the collective vision for all the actors in the food chain in a country. The presence of a Food
Safety policy (FSP) is critical to coordinated function of all the organizations charged with the
responsibility to deliver food safety. It is in this document that governments must state and
demonstrate food safety and its relation to economic and public health. The case studies of
the developing countries here demonstrate at least governments’ understanding and commit-
ment to setting up a food safety and nutrition policy.
Once a food safety policy is in place and adopted, this gives room for appropriate accompanying
legislation. The legislation must be updated, based on science; give spell out clearly the roles
and obligations of each concerned organization, and above all be enforced. For many developing
countries, the full enforcement is a missing ingredient. For food safety legislations to succeed,
they must cover all components of the food supply chain. Often in Africa, and the rest of the
developing countries, food safety legislations leave out the informal sector which is a major con-
tributor to food value chain and hence any accompanying ills.
There is great variety of indigenous foods in the developing world. Many countries do not
have standards that govern preparation and trade of these indigenous foods. Effort is put
https://www.facebook.com/myfreefoodindustrybooks/
currently through Codex Alimentarius Commission’s (CAC) Working Groups to change this.
This move should be encouraged and many countries ought to bring on the table several
of their native foods. However, the standards development process must be supported by
scientific data on nutritional and safety aspects of food which is a gap that needs to be filled.
In addition, the standards development must be responsive and internationally oriented and
the body responsible be accorded a clear mandate.
Legislation and standards that serve the intended purposes in guaranteeing food safety and
cross border trade must be science-based. WHO and FAO had earlier, in 1992, stated that risk
analysis must be the basis of any food safety framework [12], but in developing countries,
lack of expertise, low investment in the requisite infrastructure, and difficulty in collecting
own toxicological data is a hindrance to RA. This challenge is a huge one and requires col-
laborative and innovative efforts from all stakeholders. Toxicological exposure data in many
developing countries is very scanty, inaccurate, and usually not timely. To help developing
countries to conduct risk assessment, FAO/WHO studies is a great place to start but unless
these are closely related to the country’s specific needs, priority may differ from those of FAO
and WHO and depending on FAO/WHO’s focus data may take long to finally capture the
aspirations of specific countries.
3.5. Inspection
Food quality inspections demonstrate or validate the success or failure of food safety legisla-
tions. Legislations that are not enforced are not beneficial at all. This is a major setback in all
the aspects of the developing countries. Many factors contribute to this; including low status
often awarded to food safety officers, inadequate logistical support, and cumulative tasks
required of them hence intermittent attention to the task of inspection. Inadequate geographi-
cal coverage in all areas of the country by inspectors of food legislations and neglect of rural
community means that their food safety concerns often go unaddressed.
Inspections, and other aspects of food safety monitoring, depend largely on validation,
and this is partly conducted by testing of samples to ensure enforcement of legislation.
Rapid laboratory testing is also critical to implementation of food-borne illness’ outbreak
surveillance. In many cases, laboratory facilities in developing economies whether in
Asia or Africa are old, poorly equipped and with either very few personnel or with low
competency.
3.7. Capacity
Food safety legislation requires regular, planned ongoing training, and upgrading of knowl-
edge for food control officers, law enforcers, consumers and all stakeholders. Many factors
regarding food safety change from time to time. This may include status of chemicals for use
as food additives, and even specifications like microbial criteria or tolerable daily intakes.
Competent, updated and, a responsive team is required to harness these developments for the
purposes of making food safety legislations work.
One of the key hurdles to success of food safety legislations is dealing with unreported cases,
of illnesses and deaths that arise from food-related illnesses. There must be a link and a close
one at that between the food safety enforcing bodies, and the public health departments. Not
just that countries must strive to strengthen the epidemiological data collection tools, but
also the consumers ought to be well informed about the procedures and benefits of reporting
every case even to including suspected cases.
So far, there are a number of factors that make it difficult for the food safety legislation to
work “perfectly” in the developing countries. One of these reasons is minimal application
of HACCP to food processing industry and particularly because its implementation is not
a mandatory requirement. On the other hand, multinationals and some special food value
chains, particularly the export-oriented ones, have adopted HACCP or even stricter systems
as has been demanded by their customers in these markets. Of course, this varies across
countries with South Africa leading other African countries in embracing third party certifi-
cation of food companies. Developing countries must be made to understand and appreci-
ate the fact that food safety management systems that work, provide more benefits to the
citizenry and is better for the economy. These facts, however, may never have been so clearly
stated and understood by those responsible for food safety legislation, implementation, and
monitoring [2].
https://www.facebook.com/myfreefoodindustrybooks/
4.1. The two faces of developing countries’ food safety management systems
Most developing countries at least host multinational companies that are crucial and that
serve a niche market. This includes the likes of Coca Cola, Unilever, Mars Incorporated, and
Wrigley’s among others. These are companies whose food safety management systems are
extremely strict. In most cases, they are more focused on the use of their internal standards
and auditing techniques than they do rely on the inspections mounted by governments. They
have systems replete with a robust backup and huge capacity in terms of laboratories, person-
nel and necessary logistics. Unfortunately, in the developing countries, these lie and operate
side by side with the uncoordinated; unregulated street food supply chain that indeed are
greater sources of food especially for the urban, poor and middle class dwellers. The existence
of the two tier-food safety operations in the developing economies: the multinationals and
the local startups, is a phenomenon that must be harnessed as a learning point to enable food
safety be addressed to all who are affected by it.
This lack of priority means many food supply chains for the majority of the rural areas and
town dwellers are not regulated, and to compound this further, traceability mechanisms are
almost nonexistent. However, for a few commodities traded formally and internationally,
reasonable food safety parameters and legislations are in place. These commodities include;
cereals, fruits, vegetables, oil seed, cocoa, and shea nuts. Ghana Food Safety Authority is
faced with an inadequate food testing capacity quagmire. This is in reference to equipment,
personnel, and the location of the main government laboratory in Accra, serving the whole
country [5].
https://www.facebook.com/myfreefoodindustrybooks/
The various Ministries Departments and Agencies have been set up drawing form various
legislations. There is, however, a need to have these standards revised and aligned to modern
food regulations. Ghana Standards Boards’ mandate is to establish and promulgate stan-
dards. It also promotes standardization in industry and commerce thus promoting industrial
efficiency. Further, it promotes welfare, health and safety for consumers. In addition, it runs
the certification scheme, inspection of food safety operations and metrology. Government
of Ghana has several ministries involved in food safety legislation; with the ministry of
Environment and Science, Trade and Industry, Ministry of Health, and Ministry of Food and
Agriculture taking the leading roles. In the Ghanaian system standards setting formulation/
drafting and advice is divorced from the bodies involved in control and enforcement of leg-
islation. There is also separation of risk analysis and advice from the bodies mandated with
management and operationalization of the food safety system. However, Ghana has also taken
an important step in drafting the National Food Safety Action Plan (NFSAP) to restructure
food safety, agriculture, and health institutions to improve efficiency and governance. Such a
move allows for a coordinated effort among Ministries, Departments and Agencies, allowing
for smooth operations, avoiding duplication of duties, eliminating conflicts and encouraging
better enforcement of food safety legislation [5].
The legal framework mirrors that of Ghana with major components being: legislation, policy,
institutionalization (institutional framework), inspection, and laboratory testing services.
National food safety policy was established in 1999. The establishment of the food safety
policy in Nigeria set the country on a path toward well-coordinated food safety legislation. It
recognizes the roles of the public sector and that of private sector in addressing challenges of
food safety in a multisectoral model [6].
The country boasts of numerous food-related legislations. The laws focus on consumer pro-
tection, proper coordination, development of relevant policy, and priority setting in enforc-
ing food legislation. It advocates HACCP as the basis to all food production and processing
https://www.facebook.com/myfreefoodindustrybooks/
operations. The other organizations in Nigeria, charged with food safety include the Ministry
of Health, National Agency for Food and Drug Administration and Control, the Standards
Organization of Nigeria, Ministry of Agriculture and Research and Development and
Fisheries, Plant Quarantine Service, the Consumer Protection Council, Federal Ministry of
Environment and, Federal Ministry of Trade and Industry. It also recognizes the role of uni-
versity, research, and local governments in creating awareness and training of personnel for
most food safety focused agencies. The key factors to successful food legislation in Nigeria
are increased public awareness and customer education about the dangers of neglect of food
safety. There should also be better coordination among the bodies charged with responsibili-
ties for food safety. Lastly, capacity building by training of personnel, producers and regula-
tors is vital toward achieving success in implementation of food safety legislation. The SMEs
should be urged to form associations for ease of government support in terms of training and
awareness creation [6].
Kenya has over 22 Food safety-related legislations under different Departments and Agencies.
Kenya became a member of the Codex Alimentarius Commission in 1969. It has since played
some crucial functions in various Codex committees and is currently chairing the CCAFRICA
region. It has also adopted more than 100 Codex standards. Kenya has developed a National
Food and Nutrition Security Policy. Food Safety is a key pillar of the policy document and
it can be found under the subtopic of “Food Safety, Standards and Quality Control.” The
proposed National Food Safety Authority will be an innovative platform. Chiefly it will
be mandated to conduct risk assessment, an area that has been grossly underrepresented
in Kenya and the rest of the developing economies. It is also expected to promote human
health and ensure better coordination among all the multiple-stakeholders in food safety.
The Kenya’s food safety management model is integrated with several bodies across different
sectors mandated to ensure safety quality and promotion of trade for specific products in
some cases [7]. Kenya is an integral member of the East African Community (EAC). The East
African Community has been keen to harmonize several commodity standards with a total
of 42 standards recorded as having been harmonized. The thrust has been to facilitate trade
and remove barriers allowing for faster movement of goods across borders and thus reducing
food losses. Most of these achievements have been through the Working Groups on various
commodities. Despite the efforts directed to securing food safety in Kenya, foodborne ill-
nesses, and outbreaks, fraud, and other ills are still reported with regularity [7].
Having looked at some cases of developing countries in Africa, the focus shifts to understand-
ing the food safety scenarios of developing countries in Asia. Two countries that are an impor-
tant part of the Asian continent, Nepal and India are presented in a bit of depth. Developing
countries in Asia have definitely unique food safety scenarios. Nepal, for example, became a
member of WTO in the 2004, and hence food safety has acquired a reasonable interest. The
most important challenges are as follows:
https://www.facebook.com/myfreefoodindustrybooks/
Nepal is a member of CAC, WTO, FAO, and South Asian Association for regional cooperation
(SAARC). It is also a member of the World Organization for Animal Health (OIE) and Bay
of Bengal Initiative for Multi-sectoral Technical and Economic Cooperation (BIMSTEC). The
country drafted its first food legislation in 1966. This piece of legislation was called the Food
Act. The Food Act spelled out the basis for control of inspection of food premises, destruction
of nonconforming products and ensuring safety and quality of imported foods. This was then
followed by the Plant Protection Act of 1972 and Animal Health and Livestock Services Act
of 1998. The upsurge in international trade and economic liberations in Nepal in the 1990s
made food safety a priority as it became critical for acceptance of products traded internation-
ally. Initially, the focus of food safety strategies was toward end product testing. Increasingly
though, the knowledge of HACCP and other important food safety systems has resulted in
the focus moving to the “farm to fork” continuum. Food safety legislation is increasingly
based on HACCP principles even though this is not mandatory yet. Owing to the fact that
the country does not have a traceability component, effecting recalls, understanding sources
of food contamination, and hence mitigation in times of food-borne outbreaks becomes very
cumbersome and may take too long [8].
The Food safety and quality management system in Nepal is under the Ministry of Agriculture
and Cooperatives. This it done through the Department of Food Technology and Quality,
which is focused on safety and quality of food in the market and ready to eat food. While the
Department of Livestock and that of Agriculture are charged mostly with handling safety
at primary production of food. The Nepal Council for Standards and the Nepal Bureau of
Standards and Metrology are charged with standards development and implementation in
Nepal. They are the standards governing body and custodians. Nepal Council for Standards
(NCS) is mandated to approve all Nepalese standards while the Nepal Bureau of Standards
and Metrology (NBSM) functions as the secretariat that prepares the standards. NBSM has
developed and adopted more than 100 standards related to food. Through the South Asian
Regional Standards Organization (SARSO), the country is also actively involved in develop-
ment of regional standards. The Food Standards Board (FSB), advices government on stan-
dards and principles and also ensures that they are aligned to international standards. [8].
5.4.2. Food safety legislation in India and the institutional frame work
The food safety and quality management systems in India are under the mandate of the Food
Safety and Standards Authority of India (FSSAI). There exists an increased demand for safe,
https://www.facebook.com/myfreefoodindustrybooks/
high-quality food and greater choices among the Indian consumers. Food safety incidences
like the 2015-withdrawal of Maggi noodles and the governments’ surveillance of food-related
illnesses contribute to create awareness on food safety among Indian consumers. Still, over
the years, many food-borne illnesses are unreported and foodborne out brakes are errati-
cally reported. In 2006, about 13.2% of households reported food-borne illness. Food Safety
Standards Act (FSTA) of 2006 was designed to improve the overall safety of consumers and
aid advancement in international trade. Food Safety Standards Authority of India (FSSAI) is
wholly responsible for food safety matters. However, even after a decade of transitioning,
there are still overlaps of legislations between the Bureau of Indian Standards and FSSAI
especially with regard to milk. The same case is observed in fruits and vegetables as both
the FSSAI and Agricultural Marketing Standards apply yet both are based on CAC stan-
dards. These incidences confuse consumers and make it difficult for producers to distinguish
whether the regulations are mandatory or not. Finally, there also exist state-level legislations
that require compliance, and this sometimes complicates the intra-state trade [9].
5.4.2.1. The focus for better operation of food safety and management system in India
There is a need to improve capacity to enable effective inspection and monitoring of food
safety conditions in India. Prosecution and administration of food laws require to be devolved
at the state level but currently lies at national level and therefore far flung areas are hardly
reached. The country needs to improve laboratory access that currently is deficient and efforts
should be made to improve on the number of specialists in the food safety related fields. The
main focus in India’s food safety management system is on upgrading laboratories and col-
laboration between the AGMARK and the FSSAI labs and the sharing of data. This way, only
failed samples should be passed on to the national reference laboratory. The universities and
FFSAI need to train and employ food safety experts. There is a need to increase awareness
of all stakeholders especially on updated regulations. There must be increased emphasis on
training of food handlers especially among the informal and small-scale food processors and
producers. Currently, awareness is disproportionate among the rural consumers, and yet,
these consumers like everyone else deserve good quality food. Use of mass media campaigns
to target rural consumers will improve their awareness. Lastly, it is crucial to remove overlap
in responsibilities of the organizations and assign clear mandates and modes of collaboration
must be agreed [9].
GHI was launched in 2004 by the International Division of IFT and the European Federation
of Food Science and Technology (EFFoST) in collaboration with Food Safety Magazine and
Elsevier Science. GHI officially achieved the status of a nonprofit, charitable association in
2007 and is registered in Vienna, Austria. GHI aims to harmonize food safety legislations and
regulations based on solid science as datum for building consensus. GHI identifies issues
presented with justification and evidence, then prioritizes them depending on the availability
https://www.facebook.com/myfreefoodindustrybooks/
of experts as Working Groups (WGs) who then evaluate evidence provided to address the
specific issue at hand [10]. Making food safety work in the developing countries requires a
knowledgeable population. More often than not, the masses are easy to persuade and some-
times fall prey to misleading reports on food safety. Sometimes, politicians are culprits who
twist food safety issues for political gain even when the claims are not scientifically sound. A
case in point was the anti-GMO crusades conducted in Kenya in 2014–2015 leading up to the
government’s ban on production and trade of GMOs. GHI in its approach to promotion of
harmonization of food laws is addressing serious issues that could be exploited to make food
safety work in developing countries. These are discussed below.
The organization believes that meaningful consensus building regarding food safety legisla-
tions and regulations can only be achieved if stakeholders have the same understanding of
the working definitions of terms used in the area of food science and technology. This is often
taken for granted, yet GHI experts prove that even among English-speaking nations like the
UK and the USA, some terms used can markedly differ in their meaning. Take the definition of
food additives for example, this is markedly different between Canada, US, EU and Japan. GHI
has a Working Group Nomenclature on Food Safety and Quality, which had started with har-
monization of Russian and English legislations particularly with regard to definitions of terms
used in food safety and quality. Such a common definition will lead to a better understanding
among food safety experts and enhance consensus building among the developing countries as
well with the promise of better implementation of food safety legislation and regulations [11].
The GHI Working Group on Education’s aims to develop a curriculum for educating the
public and all stakeholders in the food value chain is very timely. The curriculum is targeting
food handlers and also everybody else in the food value chain. The WG aims to create training
tools and materials written in simple understandable language and including use of pictorials
targeting those who are not able to read. In addressing the knowledge gap, GHI works to
ensure that certain key messages in food safety need to be presented in the local languages
and in a manner that is understood to the media, political class, and consumers. GHI is of
the opinion that food safety legislations and regulations are often written in a manner and a
language that is difficult to understand even for trained professionals. Regulations must be
“translated” into understandable language, so that people affected can appreciate them.
GHI’s impartiality can be harnessed to help promote consensus on standards and eradicate
possible barriers and destruction of an otherwise safe food due to different countries’ legisla-
tion. Evidently, it is not for lack of consensus among scientists that differences in food safety
legislation occur but rather in the language and communication of the science to various
stakeholders. To improve this, building of capacity in terms of personnel, data management,
https://www.facebook.com/myfreefoodindustrybooks/
and risk assessment is critical. Most regulations, however, should be the same in all countries;
differences may only be needed because of specific eating patterns or genetic issues, like in
Japan and Finland where a large part of the population has no beta-galactosidase and therefore
cannot digest lactose, which makes too high concentrations of cow’s milk in food products toxic
for such people. GHI wants to harmonize the regulations so that trade barriers are removed and
food is not destroyed at the border just because the regulations between countries differ [10, 11].
The GHI is developing a Global Incident Alert Network for unauthorized food additives. In
such a case, whenever it is found that an illegal (unauthorized) substance that can harm con-
sumers is added to food, in any part the world, the individual who discovered that is tasked
with the role of alerting a dedicated committee who will then have the means and the protocol
to verify the issue within a short period of time and communicate the same to the relevant
authorities who should then take the necessary actions to correct the situation. If necessary,
this may be done anonymously, avoiding represailles by the employer. Such an initiative can
also help developing economies and enhance transparency and adherence to food safety rules
and regulations [11].
6.6. Innovations that could lead to a faster and better legislation of food safety in
the developing world
The first strategy is the implementation of the rapid alert and response system: that was pro-
posed by GHI in 2014. This system if operationalized can lead to information sharing across
the countries. Sharing strategic information could easily save lives by stopping potential
https://www.facebook.com/myfreefoodindustrybooks/
food-borne outbreaks before it happens or at least at a very early stage. Analysis of some
of the major incidents involving food-borne illnesses in the world indicate that a majority
of them would have been prevented had there been a proper reporting channel from those
who were involved but who did not talk due to fear of reprisals and possible loss of jobs [11].
Operationalization of such an alert would enthuse consumer confidence leading to increase
the economic development. Such a move would stimulate demand for high quality products
that puts the whole food safety management system of the developing countries on a higher
trajectory. Easier reporting channels, operationalization of help lines, including mobile apps
that consumers and small-scale processors can reach to seek help and meet with experts in
food safety can provide huge impact.
The second aspect that needs quick redress is regional risk assessment. Due to the nature of
funding and capacity required to make this happen, countries and institutional collaborations
in this area will help developing countries to not only cost-share requisite infrastructure, but
also the ensuing data that may be similar in a number of cases. Such an undertaking will help
countries avoid duplication of efforts, reduce unnecessary spending on infrastructure, and
enhance better collaboration on matters of risk analysis data among neighboring countries.
Third, knowledge and training of populations on the food safety basics is the most important
aspect in making food safety work best in developing economies. Food technologist and the
food technology organizations including those adhering to the IUFoST ought to play a bigger
role in pushing food safety agenda and particularly in the area of training and education. Both
IUFoST and GHI have a training component (the universal food safety curriculum) that is
envisaged to greatly improve consumer and other stakeholders’ confidence to play their role
of keeping processors and vendors in check with regard to food safety. Creation of awareness
to consumers about their rights and privileges confers them confidence and empowers them
to keep the food industry and government on toes to deliver on their food safety mandate. All
food processors and street vendors, regardless of their remote location and “small” service,
must be encouraged to register into clusters of 50–100 or even smaller groups through which
expert knowledge on basic hygiene and safe food handling practices can be passed on to them.
Fourth, every single cottage industry that is set up must be made comfortable to realize that
the food safety legislations are actually for their good and not meant to keep them away from
business. This requires a better working relationship between law enforcing bodies and these
food startups. The focus for these legislating bodies should be to midwife these businesses
first to profitability through functioning food safety systems, rather than focus on levies when
the factories can hardly break even.
Fifth, massive and urgent educational input is required in the area of abuse of additives,
or fraud in using chemicals like calcium carbide as an artificial ripening agent in fruits and
vegetables by unscrupulous traders in countries like India, and some places in Kenya [13].
Or even the use of formalin in meat preservation, or large doses of sodium metabisulphite
in meat preservation to mention a few. The use of these and other cancer causing chemicals
must be addressed to consumers and processors and their relation to cancer or the ensuing
impact of that, on households and public health explained. It is very critical to make sure that
people are made aware of the dangers of the use of such chemicals and their abuse. However,
the education must be complete by making consumers understand the relationship between
dose, exposure and the possibility of dangers particularly on additives. This way alarmistic
https://www.facebook.com/myfreefoodindustrybooks/
remarks that cause panic resulting in loss of what would essentially be good food, will be
avoided [11].
Lastly, laboratory facilities are key pillars to ensuring food safety in developing countries.
However, they require huge initial investments, high running costs, and very well-trained
personnel who are equally expensive to sustain. Developing countries should be encour-
aged to consider setting up regional centers of analysis, intra-country laboratories, shared
regional analytical capacity, and even regional training. This suggestion when implemented
will greatly lower the costs and improve access to laboratory analytical facilities. The col-
laborating countries can also realize a state-of-the-art facility thus enabling quick in-depth
analysis that is very important in case of mounting surveillance or diagnostics in cases of
disease outbreaks. The private sector involvement and support in availing laboratory analysis
and facilities should also be considered seriously as a means to bridging the gap.
Education is key area that must be addressed to provide capacity. Safety consciousness as a
culture along the entire value chain is key.Food Biosecurity or Defense is increasingly becom-
ing important, yet most developing countries are yet to begin to put policy mechanisms or
laws that govern their food value chains and protect it from fresh threats like bio-insecurity or
even bioterrorism. This also goes to developing countries’ capacity in responding to biosafety
concerns and accompanying legislation. It is high time developing countries begin to deal
with the concepts of GMOs based on evidence and perhaps exploit this area that may lead
to sufficient foods, thus eliminating the need to allow unsafe foods to enter the value chains
due to food insufficiency [11]. Even though the countries have differing opinions on GMOs,
the inadequate capacity to test for transgenics in developing economies makes it twice criti-
cal that some form of harmonized response based on evaluated and impartial evidence, be
reached to facilitate transboundary movement of GMOs.
7. Conclusions
This chapter has focused on the unique challenges to food safety legislation in some devel-
oping economies and the innovative ways in which the stake holders should approach the
subject and make it more effective. It has also presented case studies of food safety situations
in some developing countries: Asia (India and Nepal), West Africa (Ghana and Nigeria) and
East Africa. Finally, it proposes major innovations that could be put into play to make food
safety legislation work more effectively in the developing economies.
Acknowledgements
The authors sincerely wish to thank Professor Huub Lelieveld for his insights into the role
of GHI. In addition, we wish to pass our gratitude to Beena Sharma for providing invaluable
input into the food industry situation in Nepal and to Vishu Savanth for the help with data
regarding food safety situation in India.
https://www.facebook.com/myfreefoodindustrybooks/
Conflict of interest
Author details
1 Dairy and Food Science and Technology, Egerton University, Nakuru, Kenya
References
[1] FAO/WHO. Global Food Borne Disease Burden. 2015. Available from: http://www.who.
int/mediacentre/news/releases/2015/foodborne-disease-estimates/en/
[2] Leake LL. Food Safety in Africa: Food Safety and Quality Farm to Fork. February 20,
2015. Available from: http://www.foodqualityandsafety.com/article/out-of-africa/
[3] Assuring Food Safety and Quality: Guidelines for Strengthening National Food Control
Systems, FAO Food and Nutrition Paper 76, ISBN 92-5-104918-1 © FAO and WHO 2003
[4] FAO/WHO Regional Conference on Food Safety for Africa. National food safety systems
in Africa—A situation analysis (paper prepared by FAO regional office for Africa, Accra,
Ghana). Harare, Zimbabwe; October 3-6, 2005. Available from: http://www.afro.who.int/
sites/default/files/2017-06/fao_who_conf_national_food_safety_africa.pdf
[5] Sefa-Dedeh S. Ghana: Overview of Food Safety Situation in Africa-Country Position.
Presented at the Go-Global Conference; Accra. April 2009
[7] Kilonzo RM, Gathura M. The Kenya Food Control System. 2016. http://www.fao.org/
fileadmin/user_upload/agns/news_events/Pre_CCAFRICA_KenyaEN.pdf
[8] Bajagai YS. Food Safety Regulation in Nepal. 2012. Available from: http://www.foodan-
denvironment.com/2012/11/food-safety-regulation-in-nepal.html#.WhZjM19hi8E.gmail
https://www.facebook.com/myfreefoodindustrybooks/
[9] Hanzhou Yang Food Safety in India Status and Challenges (2017) TCI-TARINA Policy
Brief No. 5. May 2017. Available from: http://tci.cornell.edu/research/annual-reports/
Available at: http://www.fao.org/docrep/003/w3548e/w3548e00.htm
[10] Global Harmonization Initiative. Advocating Science-Based Food Safety Law and Trade.
2017. Available from: https://www.globalharmonization.net/
[11] Lelieveld H. Why Harmonize Food Regulations and what is needed to make it
work? Scientific Bulletin Series F. Biotechnologies. 2017;xxi:289-297. ISSN 2285-1364,
cd-rom issn 2285-5521, ISSN online 2285-1372, ISSN-l 2285-1364
[13] Consumer Federation of Kenya (COFEK). The Grave Danger of Artificially Ripened
Fruits and the Cancer Reality Check. 2014. Available from: http://cofek.co.ke/index.php/
news-and-media/823-the-grave-danger-of-artificially-ripened-fruits-and-the-cancer-
reality-check?showall=1
https://www.facebook.com/myfreefoodindustrybooks/
Chapter 4
Quorum
Quorum Sensing
Sensing Inhibition
Inhibition and
and Anti-Biofilm
Anti-Biofilm Activity
Activity of
of Traditional
Traditional Chinese
Chinese Medicines
Medicines
Additional
Additional information is available
information is available at
at the
the end
end of
of the
the chapter
chapter
http://dx.doi.org/10.5772/intechopen.74658
Abstract
Bacterial biofilm, a special stage which a large amount of bacteria are adhere to sur-
face, increase resistance to antimicrobial agents. However, all the bacteria are possibly
developed into biofilm, and bacterial biofilm is more difficult to remove from environ-
ment comparing to planktonic bacteria, which can be a strike to food industry. Many
researchers have showed that traditional Chinese medicines contribute to the reduction
of bacterial formation, since the important factor (quorum sensing) in biofilm forma-
tion is inhibited by traditional Chinese medicines. In this review, the effect of traditional
Chinese medicines and its inhibition mechanism of biofilm formation on common bacte-
rium biofilm are summarized, which provide a new direction for the removal of bacterial
biofilm.
1. Introduction
Bacterial biofilms, a bacterium growth state, which can attach to living and non-living sur-
faces, consist of a small part of bacteria and self-produced hydrated matrix of extracellular
polymeric substances. Biofilm bacteria are more resistant to antimicrobials compared with
planktonic bacteria, which cause their elimination from food processing facing great chal-
lenges [1]. The emergence of bacterial resistance to conventional antimicrobials clearly shows
that new biofilm control and removal strategies need to be proposed. Quorum sensing (QS),
is an important mechanism of bacteria protection that enable bacteria to deliver special signal
in response to changes of cell density in a certain environment, causing biofilm formation and
other virulence factors [2]. When the bacterial population densities reach a certain threshold,
© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons
© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative
Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
distribution, and reproduction in any medium, provided the original work is properly cited.
https://www.facebook.com/myfreefoodindustrybooks/
bacteria will regulate virulence, biofilm formation, luminescence and etc. Virulence expres-
sion and biofilm formation, protecting bacteria from adverse environment, are considered
to be harmful for pathogen therapy and human healthy life [3]. The normal operation of QS
system requires the participation of signal molecules, such as acylhomoserine lactone [4]. In a
word, the reagents that can inhibit QS regulation will interfere with biofilm formation, which
means that the reagent possess ability of QS inhibition (QSI) [5]. As we know, traditional
Chinese medicine has been applied for antibacterial and anti-inflammatory for many years.
However, studies on traditional Chinese medicine for drug discoveries have focused mainly
on its antibacterial property. A few attention has been given to its quorum sensing inhibition
and anti-biofilm activity [6]. Thus, the ability to disrupt this signaling process and QS signals
may be advantageous in the removal or prevention of bacterial biofilm. Different Chinese
medicine composition shows different effects on QS [7]. In order to provide references for
QSI to control biofilm formation, the effects of traditional Chinese medicines and its inhibi-
tion mechanism of biofilm formation—QS on common bacterium biofilm are reviewed in this
article.
Quorum sensing, a cell-to-cell communication system, plays a key role in biofilm formation.
When cell-to-cell signals arrive at a certain threshold, bacteria will secrete adhesion molecule
and develop into biofilm with three dimensional structures [8]. Biofilm formation is a dynamic
state which consists of (i) attachment, (ii) microcolony formation, (iii) maturation and (iv)
dispersion [9, 10]. Quorum sensing affects the whole process of biofilm development. It is
recognized that biofilms are mainly regulated by quorum sensing [11]. With quorum sens-
ing response to the environment, bacterium occurs to the secretion of signaling molecules,
the expression of the corresponding gene, and the secretion of extracellular polysaccharide
(EPS) [12]. The study showed that the content of proteins, carbohydrates, and nucleic acids
matrix increased significantly in the mature biofilm, since the biofilm matrix could protect
the embedded cells from harmful conditions [13]. It has been reported that signal molecules
play an initial role in QS system, and different signaling molecules are secreted by differ-
ent bacterium: (i) N-Acyl homoserine lactones (AHLs), which are synthesized by LuxI-type
enzyme, are mainly functioned in gram-negative bacterium, such as Aeromonas hydrophila [14]
and Pseudomonas aeruginosa [15]. Most of gram-negative bacteria generate and detect several
autoinducers, including C4-HSL, 3OH C4 HSL, lsovalery-HSL and etc. The chain length of
AHLs can vary from 4 to 18 carbons, where oxidation status of the third carbon can change
from fully reduced to fully oxidized [16]. The regulation of AHLs controls a series of target
functions, such as biofilm formation, motility, fluorescence synthesis, expression of virulence
genes and production of virulence factors [17]. When the concentration of signals arrives at
a certain threshold, AHLs automatically enter the bacterium, binding to the cognate receptor
to form an autoinducer-receptor complex, which causes the expression of functional gene
(Figure 1). AHLs defective P. aeruginosa produced less virulence factors and less biofilm, and
are diffusible signal molecules that may cause infections in human [16]. (ii) Gram-positive
https://www.facebook.com/myfreefoodindustrybooks/
bacterium is mainly regulated by autoinducing peptides (AIPs) [18]. Since AIPs cannot pass
through the cytoderm by itself, bacterium response to the environment through two-com-
ponent protein, transmit the signal to the cell. The activation of the receptor kinase takes
place when reaching the threshold level. The sensor kinase protein can be activated and then
phosphorylate the response regulator protein, which bind to the target promoter, and subse-
quently transcriptional activates the genes for the two-component regulatory system, result-
ing in autoinduction in a dynamic range [19]. The production of AIP is expressed by relevant
genes, then releasing out of extracellular membrane (Figure 1). (iii) Autoinducer-2 (AI-2), a
signal molecule produced by LuxS, widely existed in both gram-positive and gram-negative
bacterium. AI-2, which involved in regulating the many bacterium biofilms, was thought to
be a universal signal molecule [20]. It has been demonstrated that regulation of AI-2 plays
a significant role in biofilm formation in many kinds of bacteria. DPD is known to undergo
intra-molecular cyclization to form distinct biologically active signal molecules, which col-
lectively called AI-2. Thus, the AI-2 signal should not be recognized as a single structure, but
a family of isomers, each bacterium representing a different mode of perception [21]. (2S,
4S)-2-methyl-2, 3, 3, 4 tetrahydroxytetrahydrofuryl borate (S-THMF-borate) is the AI-2 signal
of Vibrionaceae, while S. Typhimurium produces (2R, 4S)-2-methyl-2, 3, 3, 4- tetrahydroxytetra-
hydrofuran (R-THMF) as AI-2 signal. Quorum sensing pathways of AI-2 differs due to differ-
ent bacterial species [22]. Most of the gram-positive bacteria are sensitive to penicillin, while
gram-negative bacteria are not usually influenced by penicillin. Thus, the application of QS
inhibitor is of great significance in biofilm inhibition and bacteria removal [23]. The process of
QS can be disrupted by different mechanisms: (i) inhibiting the production of QS signal mol-
ecules (AHL, AI-2 and AIP), (ii) reducing the activity of QS signal molecules, (iii) degradation
https://www.facebook.com/myfreefoodindustrybooks/
of QS signal molecules, (iv) designing the analogues of signal molecules as QSI [24]. The
regulation of QS may play a dual role on bacteria. Interferon with QS process can prevent
bacteria from biofilm protection and virulence expression, but it is limited that antibiotic---
antimicrobial cannot disrupt QS regulation. Traditional Chinese medicine is popular as QS
inhibitors to disrupt QS signals, and thereby destroy bacterial biofilm and virulence expres-
sion without killing bacterium itself [25].
Staphylococcus is one of the kinds as common and representative gram positive bacterial
pathogens in the research of QS and biofilm development. Quorum-sensing regulation plays
a vital role in the biofilm formation of many bacterial pathogens [26]. As previous mentioned,
LuxS emzyme participated in the synthesis of AI-2, which had an indispensable impact on
biofilm development of staphylococci quorum-sensing system. ΔluxS mutant strain shows
more biofilm formation in vitro and enhanced virulence in Staphylococcus epidermidis of bio-
film-associated infection. The inhibitors of luxS expression in vitro can be a promising QS
inhibitor for the prevention of biofilm and virulence [27]. Burdock leaf ethanol fraction sup-
pressed biofilm formation of S. aureus and Listeria monocytogenes. It was found that burdock
leaf ethanol fraction (1.25 mg/ml) entirely inhibited (100%) the S. aureus biofilm formation,
which was lower than MIC of the fraction. GC–MS/MS analysis shows that eight active com-
pounds from burdock leaf fraction interfered with quorum sensing regulation and disrupted
the composition of signaling molecules, thereby affecting the function of the quorum sensing
system and disturbing biofilm formation. Eight active compounds should be exactly identi-
fied for real applications [28]. Later study analyzed 34% ethanol elution fraction of burdock
leaf, found that 10 active compounds exhibited anti-biofilm activity, including chlorogenic
acid, caffeic acid, p-coumaric acid, quercetin, ursolic acid, rutin, luteolin, crocin, benzoic acid
and tenacissoside I. According to the metabolic fingerprints of burdock leaf fractions, chlo-
rogenic acid and quercetin were demonstrated to be a potential antibiofilm of Salmonellaty
phimurium compounds in burdock leaf [29]. S. aureus strains were tested for a relation between
the ability of S. aureus attachment in polystyrene and the agr quorum-sensing system phe-
notype. Less of agr-positive strains cause biofilm formation, showing a vital impact of agr
on biofilm development. Inhibitor of agr is as quorum-sensing blockers for S. aureus preven-
tion [30]. The emergence of methicillin resistant S. aureus (MRSA) caused antibiotic invalidity
and required new drugs for treating infectious diseases. Chamaecyparis obtusa essential oil
had antibacterial effect against MRSA, finding agrA expression was inhibited with C. obtusa
essential oil. Thus, C. obtusa essential oil regulates quorum-sensing to inhibit MRSA biofilm
formation [31]. Study shows a certain concentration of baicalein (32 μg/mL and 64 μg/mL)
clearly inhibited biofilm formation in vitro, and the combined use of vancomycin and baica-
lein generally enhance disruption of biofilms. 32 μg/mL and 64 μg/mL baicalein downregulate
the quorum-sensing system regulators agrA and affecting biofilm development. Therefore,
baicalein can inhibit the quorum sensing system while enhancing the permeability of vanco-
mycin and reducing the production of staphylococcal enterotoxin A and α-hemolysin as well
https://www.facebook.com/myfreefoodindustrybooks/
as inhibiting S. aureus biofilm formation. It is predicted that baicalein will be a novel drug
candidate for S. aureus infections [32]. There are differences on the combination of ethanolic
extracts of eight traditional Chinese medicines and four antibiotics. The ethanolic extracts of
Isatis tinctoria, Scutellaria baicalensis and Rheum palmatum enhance the antimicrobial activity
of four antibiotics on resistance of methicillin resistant S. aureus [33]. In summary, traditional
Chinese medicine extracts inhibit QS and biofilm formation by controlling QS molecular sig-
nals, and usually regulating the cell to cell QS---AI-2. Recently, scientists deeded crude extract
of anti-QS activity and Chinese herbal medicinal ingredient should be taken in-depth study
in the future.
Previous studies have demonstrated that a large majority of traditional Chinese medicine
show great sensitivity to gram negative bacteria QS and biofilm. It is well-known on the
research of QS that Chromobacterium violaceum CV026 and P. aeruginosa PA01 is regard as two
biomonitor strains to detect QSI on traditional Chinese medicine [34]. Twenty kinds of tradi-
tional Chinese medicine plants generally used in South-East Asia were screened for QS inhibi-
tion using two biomonitor strains, P. aeruginosa and C. violaceum CV026 PA01—gram negative
bacteria. C. violaceum CV026, which can produce AHL signal molecule, produce purple pig-
ment. P. aeruginosa PA01 control swarming through QS regulation. Thus, the change of purple
pigment and swarming can be used to reflect the regulation of QS. This study found that 8
kinds of traditional Chinese medicine extracts possess QSI ability in C.violaceum CV026, and 4
kinds of traditional Chinese medicine extracts possess QSI ability in PA01. Lilium brownie and
Panax pseudoginseng extracts possess QSI ability both in PA01 and CV026, which are meaning-
ful for various biofilm inhibitions. The findings revealed that there are rich sources of plants
on traditional Chinese medicine that contain components are able to break QS and QS-related
virulence factors. However, the specific compounds and mechanism should be applied into
deeper study [35]. Four organic solvents (n-hexane, DCM, methanol and 50% v/v acetone)
were used to extract Ficus carica and Perilla frutescens in another study. The tests of C. violaceum
CV026 and P. aeruginosa PA01 finds the extract of F. carica with dichloromethane and of P. fru-
tescens with MeOH show the obvious inhibition of QS activity. Both of them display anti-QS
ability. It is not sure the ingredient and inhibition concentration of crude extracts [36]. Study
found that methanolic extract of Phyllanthus amarus interrupted the ability of C. violaceum
CV026 to response towards exogenously supplied N-hexanoylhomoserine lactone, exhibiting
the anti-quorum sensing activity. In addition, as the concentrations of the methanolic extracts
of P. amarus increased, swarming motility, pyocyanin production and lecA: lux expressions
in P. aeruginosa PA01 were reduced. Methanolic extracts of P. amarus may serve as promis-
ing anti-pathogenic drugs due to its anti-quorum sensing properties [37]. Ginseng aqueous
extract at concentrations of 0.5–2.0% significantly inhibited P. aeruginosa biofilm formation.
Oral administration of ginseng extracts in mice did not affect phagocytosis of a PAO1-filM
mutant. According to previous study, Ginseng aqueous extract may prevent biofilm develop-
ment by the regulation of QS [38]. Quorum sensing inhibitors could inhibit biofilm formation,
https://www.facebook.com/myfreefoodindustrybooks/
but the exact role of quorum sensing in various stages of biofilm attachment, maturation, and
dispersal is not clear. In vitro the combination of antibiotic and QS inhibitor generally lead
to increase bacterial lethality, compared with treatment by an antibiotic alone. The combina-
tion of tobramycin and baicalin hydrate reduced the burkholderia cenocepacia infection. Among
this study, baicalin hydrate targets the acylhomoserine lactone-based QS system present in B.
cepacia complex organisms [39]. Curcumin from Curcuma longa (turmeric), an anti-QS agent,
was demonstrated to inhibit the biofilm formation of E. coli, P. aeruginosa PAO1, Proteus mira-
bilis and Serratia marcescens, interfering with their QS systems. The treatment with curcumin
may attenuate the QS-dependent factors, including exopolysaccharide production, alginate
production, swimming and swarming motility of uropathogens. Curcumin is as a QSI for
urinary tract treatment [40]. Three anthocyanidins (pelargonidin, cyanidin and delphinidin)
decreased the formation of P. aeruginosa PAO1 biofilm at low sub-MIC (0.125 MIC). Comparing
with ampicillin and streptomycin, delphinidin show the most active of anti-biofilm activity.
Water-soluble delphinidin structure could be used for the design of the novel and more effec-
tive anti-biofilm agents [41]. N-acylhomoserine lactone (AHL)-based QS plays vital role in
biofilm formation and virulence expression. Three Chinese herbal ingredients namely are
salicylic acid, tannic acid and trans-cinnamaldehyde, are as AHL synthase inhibitors to inhibit
quorum sensing. Natural products targeting AHL synthase may provide anti-QS signal syn-
thesis for prevention of pathogenic bacteria [42]. Traditional Chinese herbs could inhibit key
biofilm-associated genes in P. aeruginosa. Herba patriniae extract showed significantly reduc-
tion on the biofilm formation and change the structure of the P. aeruginosa biofilms. Further
studies showed H. patriniae extract promoted its swarming motility. The possible inhibition
mechanism is that H. patriniae may regulate QS to control bacterial biofilm and swarming [43].
Study found that 30 mg/ml of Melia dubia seed ethanolic extract inhibited biofilm, hemolysis
and swarming motility by 92.1, 20.9, and 48.52%, suggesting that the ethanolic extract pos-
sessed potency to restrain quorum sensing of uropathogenic E. coli [5]. It has been demon-
strated that quorum sensing quenching effect exists in traditional Chinese medicine plants,
foreseeing the tremendous prospect of QSI application on traditional Chinese medicine [44].
The concrete mechanism of traditional Chinese herbs is unsure, but some chemical compo-
nents have been found in traditional Chinese herbs. It is believed that most of traditional
Chinese medicines are as promising QS inhibitors for bacterial infection and biofilm disrup-
tion. Traditional Chinese medicines may be a novel material for infectious diseases and food
safety with antibiotic.
To sum up the above arguments, most researches of QSI on gram negative bacteria have
been taken into deep consideration. It has been demonstrated that P. aeruginosa PA01 and C.
violaceum CV026 can detect QSI of gram negative bacteria. Furthermore, the active constituent
of traditional Chinese medicines also has been shown in the research. Most of active constitu-
ents are extracts of water-alcohol, since aqueous extracts are more effective on biofilm inhibi-
tion than organic solvent. Panax pseudoginseng extracts on mouse test and experiment in vitro
https://www.facebook.com/myfreefoodindustrybooks/
found that aqueous extracts control biofilm formation by the regulation of QS [45]. In addi-
tion, methyl alcohol and ethyl alcohol, especially ethanol extract, are regarded as the common
solvent to extract traditional Chinese medicines. Anthocyanidins, salicylic acid, baicalin and
curcumin show inhibition of QS and QS-dependent biofilm, which can be assumed traditional
Chinese medicines plants containing these components control QS regulation (Table 1). Now
the combination of these components and antibiotic to kill bacteria are more effective that
single antibiotic, so it is hopeful that the components can treat bacterial infection efficiently.
Except for Staphylococcus, QSI on other gram negative bacteria is less mentioned. Ethanol
extract of traditional Chinese medicines also possess strongly anti-biofilm property, but the
mechanism of QS to biofilm inhibition is still unsure. Similarly, the active constituents on
gram positive bacteria are flavonoid and organic acid, such as chlorogenic acid, chrysophanic
acid and baicalein (Table 1). In summary, it is found that flavonoids extracted on TCM can be
used as a hopeful QS inhibitor. Some of organic acid and essential oil not only reveal antibac-
terial property, but also show biofilm inhibition. Thus, it is believed that traditional Chinese
medicines containing these components can hinder QS regulation and biofilm formation, and
the plants with anti-QS and anti-biofilm property should be taken into consideration.
6. Conclusion
Different components of traditional Chinese medicine also exert anti-QS activities on the
gram-positive bacteria and gram-negative bacteria. Gram-negative bacteria seems sen-
sitive to QS inhibitor, since C. violaceum CV026 and P. aeruginosa PA01 are usually as
biomonitor strains for detection of QSI [46]. Common pathogenic bacteria, such as S.
epidermidis [47], S. aureus [48], E. coli [49] and P. aeruginosa [50], are mainly interfered
with biofilm development and toxicant release by QS regulation. It has been found that
the combination of traditional Chinese medicine and antibiotics could improve the anti-
bacterial activity and remove bacterial biofilm effectively. Nowadays most of traditional
Chinese medicines are screened for a pathogenic bacterium QSI. However, less reports
show a broad spectrum QS activity on traditional Chinese medicines [51]. Therefore,
https://www.facebook.com/myfreefoodindustrybooks/
screening traditional Chinese medicine ingredients with anti-QS function, can treat the
common pathogens biofilm and remove drug-resistant bacteria, being promising drugs
for antibiotics auxiliary treatment. Antibiosis activity has been shown in many Chinese
medicine ingredients, but now antibiotics are still the priority drugs for clinic treatment of
infectious diseases. The following problems are for the better development of traditional
Chinese medicine in the future. The first step is to explore QS mechanism of traditional
Chinese medicine, enable traditional Chinese medicine ingredients inhibit the specific
pathogens biofilm this phenomenon reach a theoretical stage thus people can have a more
profound understanding. Secondly, the researches of traditional Chinese medicine still
experience in a basically experimental stage. Experimental in vivo and clinical trials on
traditional Chinese medicine should be strengthened, only which can lead to a further
application. The last but not least, the specific efficacy of traditional Chinese medicine
should be confirmed, and try to use new methods on extracting them. Since traditional
Chinese medicine work usually by complex inducers, novel methods like metabolic engi-
neering can be applied to increase the active ingredient dramatically in the meanwhile
decrease the cost. It is hoped that traditional Chinese medicine could be used for food
safety in the food industry.
Acknowledgements
This work has been supported by Science Research Fund of Wuhan Institute of Technology
(17QD01) and the National Natural Science Foundation of China (31501582).
Conflict of interest
Author details
References
[1] Zhao XH, Wang L, Chu J, Li YY, Li YM, Xu ZB, Li L, Shirtliff ME, He XW, Liu Y, et al.
Rapid detection of Vibrio Parahaemolyticus strains and virulent factors by loop-mediated
isothermal amplification assays. Food Science and Biotechnology. 2010;19(5):1191-1197
[2] Li YH, Tian X. Quorum sensing and bacterial social interactions in biofilms. Sensors.
2012;12(3):2519-2538
[3] Bhardwaj AK, Vinothkumar K, Rajpara N. Bacterial quorum sensing inhibitors: Attrac-
tive alternatives for control of infectious pathogens showing multiple drug resistance.
Recent Patents on Anti-Infective Drug Discovery. 2013;8(1):68
[4] Zan J, Yue L, Clay F, Hill RT. Acyl-Homoserine lactone quorum sensing in the Roseo-
bacterClade. International Journal of Molecular Sciences. 2014;15(1):654-669
[5] Zhao XH, Li YM, Park M, Wang J, Zhang YH, He XW, Forghani F, Wang L, Yu GC, Oh
DH. Loop-mediated isothermal amplification assay targeting the femA gene for rapid
detection of Staphylococcus aureus from clinical and food samples. Journal of Microbiology
and Biotechnology. 2013;23(2):246-250
[6] Chong-Lek K, Choon-Kook S, Yin WF, Ying TL, Thiba K, Meng CY, Chan KG. Plant-
derived natural products as sources of anti-quorum sensing compounds. Sensors.
2013;13(5):6217
[7] Zhao X, Lin C-W. Rapid label-free visual detection of KRAS mutations using peptide
nucleic acid and unmodified gold nanoparticles. RSC Advances. 2017;7(77):48554-48560
[8] Xu ZB, Li L, Zhao XH, Chu J, Li B, Shi L, Su JY, Shirtliff ME. Development and appli-
cation of a novel multiplex polymerase chain reaction (PCR) assay for rapid detection
of various types of staphylococci strains. African Journal of Microbiology Research.
2011;5(14):1869-1873
[9] Zhao T. Biofilm formation of foodborne pathogens and their control in food processing
facilities. Journal of Food: Microbiology, Safety and Hygiene. 2016;1:110
[10] Zhao X, Zhao F, Wang J, Zhong N. Biofilm formation and control strategies of foodborne
pathogens: Food safety perspectives. RSC Advances. 2017;7(58):36670-36683
[11] Waters CM, Bassler BL. Quorum sensing: Cell-to-cell communication in bacteria. Annual
Review of Cell and Developmental Biology. 2005;21(21):319
[12] Zhao XH, Wang L, Chu J, Li YM, Li YY, Xu ZB, Li L, Shirtliff ME, He XW, Liu Y, et al.
Development and application of a rapid and simple loop-mediated isothermal ampli-
fication method for food-borne salmonella detection. Food Science and Biotechnology.
2010;19(6):1655-1659
https://www.facebook.com/myfreefoodindustrybooks/
[13] Dickschat JS. Quorum sensing and bacterial biofilms. Natural Product Reports. 2010;
27(3):343
[14] Ponce-Rossi ADR, Pinto UM, Ribon ADOB, Bazzolli DMS, Vanetti MCD. Quorum sens-
ing regulated phenotypes in Aeromonas Hydrophila ATCC 7966 deficient in AHL pro-
duction. Annals of Microbiology. 2016;66(3):1117-1126
[15] Meizhen W, Schaefer AL, Dandekar AA, Greenberg EP. Quorum sensing and policing of
Pseudomonas aeruginosa social cheaters. Proceedings of the National Academy of Sciences
of the United States of America. 2015;112(7):2187-2191
[17] Liu JY, Zhou R, Li L, Peters BM, Li B, Lin CW, Chuang TL, Chen DQ, Zhao XH,
Xiong ZY, et al. Viable but non-culturable state and toxin gene expression of entero-
hemorrhagic Escherichia Coli 0157 under cryopreservation. Research in Microbiology.
2017;168(3):188-193
[18] Tal-Gan PDY, Ivancic M, Cornilescu G, Yang T, Blackwell PDHE. Highly stable, amide-
bridged autoinducing peptide analogues that strongly inhibit the AgrC quorum sensing
receptor in Staphylococcus aureus. Angewandte Chemie (International Ed. in English).
2016;55(31)
[20] Zhu P, Peng H, Ni N, Wang B, Li M. Novel AI-2 quorum sensing inhibitors in Vibrio
Harveyi identified through structure-based virtual screening. Bioorganic & Medicinal
Chemistry Letters. 2012;22(20):6413-6417
[21] Xavier KB, Miller ST, Lu W, Kim JH, Rabinowitz J, Pelczer I, Semmelhack MF, Bassler
BL. Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in
enteric bacteria. ACS Chemical Biology. 2007;2(2):128
[22] Guo M, Gamby S, Zheng Y, Sintim HO. Small molecule inhibitors of AI-2 Signaling
in bacteria: State-of-the-art and future perspectives for anti-quorum sensing agents.
International Journal of Molecular Sciences. 2013;14(9):17694-17728
[24] Amara N, Krom BP, Kaufmann GF, Meijler MM. Macromolecular inhibition of quorum
sensing: Enzymes, antibodies, and beyond. Chemical Reviews. 2011;111(1):195-208
https://www.facebook.com/myfreefoodindustrybooks/
[25] Ding X, Ding J, Zhao J, Guo Y, Liu Q. Research progress on resistance mechanisms of
pseudomonas Aeruginosa and treatment from traditional Chinese medicine. World Chinese
Medicine. 2016
[26] Boyaci H, Shah T, Hurley A, Kokona B, Li Z, Ventocilla C, Jeffrey PD, Semmelhack MF,
Fairman R, Bassler BL. Structure, regulation, and inhibition of the quorum-sensing sig-
nal integrator LuxO. PLoS Biology. 2016;14(5):e1002464
[27] Xu L, Li H, Vuong C, Vadyvaloo V, Wang J, Yao Y, Otto M, Gao Q. Role of the luxS
quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis.
Infection and Immunity. 2006;74(1):488-496
[28] Lou Z, Hong Y, Liu Y, Song X, Ai L, Wang H, Jiao A, Tang Y. Effect of ethanol fraction
of burdock leaf on biofilm formation and bacteria growth. European Food Research and
Technology. 2014;239(2):305-311
[29] Tang Y, Lou Z, Yang L, Wang H. Screening of antimicrobial compounds against
Salmonellaty phimurium from burdock (Arctium Lappa) leaf based on metabolomics.
European Food Research and Technology. 2015;240(6):1203-1209
[30] Vuong C, Saenz HL, Götz F, Otto M. Impact of the agr quorum-sensing system on adher-
ence to polystyrene in Staphylococcus aureus. Journal of Infectious Diseases. 2000;182(6):1688
[31] Kim ES, Kang SY, Kim YH, Lee YE, Choi NY, You YO, Kim KJ. Chamaecyparis Obtusa
essential oil inhibits methicillin-resistant Staphylococcus aureus biofilm formation and
expression of virulence factors. Journal of Medicinal Food. 2015;18(7):810
[32] Yan C, Liu T, Ke W, Hou C, Cai S, Huang Y, Du Z, Hong H, Kong J, Chen Y. Baicalein
inhibits Staphylococcus aureus biofilm formation and the quorum sensing system In vitro.
PLoS One. 2016;11(4):e0153468
[33] Yang ZC, Wang BC, Yang XS, Wang Q, Ran L. The synergistic activity of antibiotics
combined with eight traditional Chinese medicines against two different strains of
Staphylococcus aureus. Colloids and Surfaces. B, Biointerfaces. 2005;41(2-3):79-81
[34] Zhu H, He CC, Chu QH. Inhibition of quorum sensing in Chromobacterium violaceum
by pigments extracted from Auricularia auricular. Letters in Applied Microbiology.
2011;52(3):269-274
[35] Yeo SSM, Tham FY. Anti-quorum sensing and antimicrobial activities of some tradi-
tional Chinese medicinal plants commonly used in South-East Asia. Malaysian Journal
of Microbiology. 2012;8(1)
[36] Sun S, Li H, Zhou W, Liu A, Zhu H. Bacterial quorum sensing inhibition activity of
the traditional Chinese herbs, Ficus Carica L. and Perilla Frutescens. Chemotherapy.
2014;60(5-6):379
[37] Priya K, Yin WF, Chan KG. Anti-quorum sensing activity of the traditional Chinese herb,
Phyllanthus amarus. Sensors. 2013;13(11):14558-14569
https://www.facebook.com/myfreefoodindustrybooks/
[38] Wu H, Lee B, Yang L, Wang H, Givskov M, Molin S, Høiby N, Song Z. Effects of gin-
seng on Pseudomonas aeruginosa motility and biofilm formation. FEMS Immunology and
Medical Microbiology. 2011;62(1):49-56
[39] Brackman G, Cos P, Maes L, Nelis HJ, Coenye T. Quorum sensing inhibitors increase
the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrobial
Agents and Chemotherapy. 2011;55(6):2655
[40] Packiavathy IASV, Priya S, Pandian SK, Ravi AV. Inhibition of biofilm development of
uropathogens by curcumin – An anti-quorum sensing agent from Curcuma longa. Food
Chemistry. 2014;148(3):453-460
[41] Pejin B, Ciric A, Markovic JD, Glamoclija J, Nikolic M, Sokovic M. An insight into anti-
biofilm and anti-quorum sensing activities of the selected anthocyanidins: The case
study of Pseudomonas aeruginosa PAO1. Natural Product Research. 2016:1-4
[42] Chang CY, Krishnan T, Wang H, Chen Y, Yin WF, Chong YM, Tan LY, Chong TM, Chan
KG. Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone
synthase as druggable target. Scientific Reports. 2014;4:7245
[43] Fu B, Wu Q, Dang M, Bai D, Guo Q, Shen L, Duan K. Inhibition of Pseudomonas aerugi-
nosa biofilm formation by traditional Chinese medicinal HerbHerba patriniae. BioMed
Research International. 2017;2017
[44] Ravichandiran V, Shanmugam K, Solomon AP. Screening of SdiA inhibitors from Melia
dubia seeds extracts towards the hold back of uropathogenic E. Coli quorum sensing-
regulated factors. Medicinal Chemistry. 2013;9(6):819
[45] Wu H, Lee B, Yang L, Wang H, Givskov M, Molin S, Høiby N, Song Z. Effects of ginseng
on Pseudomonas aeruginosa motility and biofilm formation. Fems Immunology & Medical
Microbiology. 2011;62(1):49
[46] Fitriani A, Ayuningtyas DP. Kusnadi: Inhibition of quorum sensing in Chromobacterium
violaceum cv026 by violacein produced by Pseudomonas aeruginosa. Journal of Experimental
Biology & Agricultural Sciences. 2016
[47] Brackman G, Breyne K, De RR, Vermote A, Van NF, Meyer E, Van CS, Coenye T. The quo-
rum sensing inhibitor Hamamelitannin increases antibiotic susceptibility of Staphylococcus
aureus biofilms by affecting peptidoglycan biosynthesis and eDNA release. Scientific
Reports. 2016;6:20321
[48] Yu D, Zhao L, Xue T, Sun B. Staphylococcus aureus autoinducer-2 quorum sensing decreases
biofilm formation in an icaR-dependent manner. BMC Microbiology. 2012;12(1):288
[50] Smith RS, Iglewski BH. P. aeruginosa quorum-sensing systems and virulence. Current
Opinion in Microbiology. 2003;6(1):56-60
[51] Chen Y, Yao F, Ming K, Wang D, Hu Y, Liu J. Polysaccharides from traditional Chinese
medicines: Extraction, purification, modification, and biological activity. Molecules.
2016;21(12):1705
https://www.facebook.com/myfreefoodindustrybooks/
Chapter 5
Neli Ermenlieva,
Neli Ermenlieva, Gabriela
Gabriela Tsankova,
Tsankova,
Darina Naydenova, Tatina T.T. Todorova,
Todorova,
Dayana Tsankova and Emilia Georgieva
Additional information
Additional information is
is available
available at
at the
the end
end of
of the
the chapter
chapter
http://dx.doi.org/10.5772/intechopen.75965
Abstract
Bioterrorist attacks are usually associated with airborne infections because of their easy
dissemination and maximal effect on the human population. However, foodborne patho-
gens represent potential bioterrorist weapons, as the consumption of safe food affects
every individual in the society. Most of the foodborne microorganisms can be readily iso-
lated from natural sources and can cause severe outbreaks with a number of hospitalized
persons. Biological agents, which may contaminate food products, are bacteria, viruses,
yeasts, parasites, or chemical substances with microbial origin. They cause more than
200 diseases—ranging from diarrhea to cancers. Typical symptoms of food poisoning are
abdominal cramps, nausea, vomiting, upset stomach, diarrhea, fever, dehydration, and
others. Most isolated bacterial agents responsible for foodborne infections include bac-
teria from genera such as Salmonella, Shigella, Bacillus, Clostridium, Listeria, Campylobacter,
Escherichia, Staphylococcus, Vibrio, Enterobacter, and Yersinia. In this chapter, we discuss the
bacterial species causing food poisoning in the context of a potential bioterrorist attack.
We review in a concise manner their morphological and biochemical characteristics, as
well as the treatment and possible prevention measures. Popular examples of attacks
with food poisoning agents and their impact on the society are also given.
1. Introduction
Bioterrorism refers to the use of infectious agents or other harmful biological or biochemi-
cal substances for terroristic purposes. Usually, the measures against bioterrorist attacks are
© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons
© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative
Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
distribution, and reproduction in any medium, provided the original work is properly cited.
https://www.facebook.com/myfreefoodindustrybooks/
focused on the aerosol infections, as airborne microorganisms can easily affect many people
and lead to maximal morbidity when entering the respiratory tract. However, in some cases,
the aim of a bioterrorist attack is not to achieve high lethality but also to produce fear, panic,
and chaos in the community. In this context, the intentional dissemination of bacterial agents
causing food poisoning is a potential bioterrorist threat.
The first attempts to use the pathogenic properties of some microorganisms in a destruc-
tive manner dated many centuries ago. In particular, bacteria causing food poisoning were
extremely suitable as many of them (plague, cholera) were epidemically spread in the past
and easily available for war and bioterrorist purposes. The plague is a typical example with
many naturally occurred outbreaks and one well-documented intentional epidemic in human
history: in 1346, during the Tatar siege of Caffa on the Crimean Peninsula, infected corpses
have been catapulted in the city to cause a local outbreak which finally resulted in one of the
most devastating epidemics in Europe—the Black Death [1].
In the beginning of the twentieth century, biological agents were used on a scientific basis by
different national governments for war purposes. The effects of anthrax, cholera, glanders,
dysentery, tetanus, typhus, salmonella, tularemia, and typhus with pox were less or more
successfully studied and tested on animals and humans [1–3]. Comprehensive studies on the
use of botulinum toxin were also undertaken during World War II, especially by the US gov-
ernment which intended to use prostitutes to assassinate Japanese officers by gelatin capsules
loaded with botulinum toxin [4].
In the next decades, despite the ratification of a Convention on the prohibition of the develop-
ment, production and stockpiling of bacteriological (biological) and toxin weapons and on
their destruction (usually referred to as the Biological Weapons Convention) in 1972–1975,
most of the countries have continued to work and design new biological agents to be used as
weapons in eventual war conflicts. In such a way, fundamental knowledge was gained and it
was just a question of time to be used for destructive purposes.
At the end of the twentieth century, the changed geopolitical situation resulted in less con-
frontation between the countries but in the appearance of different political, religious, or
nationalistic extremist movements with well-qualified and motivated members, prepared to
use the available knowledge and technologies. Between 1990 and 1995, at least three bioter-
rorist attacks with botulinum neurotoxin failed in Japan [5]. During the same decade, the
international community found thousands of litters of botulinum toxin, anthrax, and aflatoxin
in Iraq that were ready to be used as mass destruction weapons [6].
The biggest bioterrorist attack in the USA occurred in 1984 with a foodborne pathogen—
Salmonella typhimurium—which was used to contaminate salad bars in restaurants in Oregon
[7]. Members of the religious commune “Bhagawan Shree Rajneesh” tried to sabotage the
local elections and succeeded in infecting 751 persons.
The most popular bioterrorist attacks occurred in 2001 over the whole territory of the USA
when spores of Bacillus anthracis were sent via post letters to different governmental and pub-
lic institutions. As a result of these attacks, 22 persons were infected and 5 of them died.
In the twenty-first century, with the enlarged terrorist activity, the preparedness of society for
bioterrorist attacks, including intentional food poisoning, should also expand to guarantee
quick response and adequate action. The main foodborne pathogens with a potential to be
used as a biological weapon should be known, as well as their prevention and treatment.
The Centers for Disease Control and Prevention (CDC) recognizes three categories of biologi-
cal agents in respect of bioterrorism [9]:
• Category A: These are high-priority agents posing a risk to national security because of
their easy dissemination, high mortality rates, and high public health impact. They require
special action for public health preparedness.
• Category B: These are the second highest priority agents. They have moderately easy dis-
semination, moderate morbidity rates, and low mortality rates. These microbes require
specific enhancements of diagnostic capacity and enhanced disease surveillance.
Category В
Category C
Not cited
Table 1. Categories of foodborne bacteria (and their corresponding diseases) as possible bioterrorist agents (according to [9]).
https://www.facebook.com/myfreefoodindustrybooks/
• Category C: These include the third highest priority agents, which are emerging pathogens
that could be easily engineered. They have potential for high morbidity and mortality rates
and major health impacts.
Table 1 shows which foodborne bacterial pathogens fall into these three categories of potential
biological weapons. Bacillus anthracis is the bacterium most likely to be used as a bioterrorist agent
because its spores are widely spread in nature and it easily grows under nonspecific conditions in
the laboratory. Anthrax spores can be released at any place as aerosols but also can be put in food
and drink. However, airborne route of transmission is more dangerous for the society and there-
fore preferred for terroristic purposes. Historically no intentional cases of foodborne transmission
of anthrax are cited and as the objective of this chapter is to summarize food poisoning agents as
potential biological weapons, Bacillus anthracis should not be considered further in the text.
Currently, botulinum toxin is considered as the strongest toxic substance in the world—1 g
may cause the death of millions of people. The symptoms of botulism, as well as the bac-
terial characteristics, classify Clostridium botulinum in category A of biological agents with
the potential to be used as a terroristic tool (Table 1). The disease is associated with severe
neuromuscular damage, urgent need of hospitalization, and intubation. In the case of massive
infection, the hospital infrastructure of any country could not provide adequate care for all
patients. In addition, the bacterium has a high morbidity and relatively easy cultivation and
transport. The transmission via aerosols is considered to be the most dangerous in a potential
bioterrorist attack, but the alimentary mechanism of infection spread is also possible, as it is
historically well known although logistically limited [5, 6].
The typical clinical manifestation of descendent flaccid paralysis put botulism in a specific
category but misdiagnosis is common and represents an additional issue in a hypothetical
bioterrorist act. In 1985, a major outbreak of botulism in Vancouver had remained unrecog-
nized for a long time. Twenty-eight individuals were infected with contaminated restaurant
food but were hospitalized with different diagnoses before the proper epidemiological inves-
tigation [14].
used for the attack, the strain characteristics, and the environmental conditions. Symptoms
will appear 1–6 days after the exposition and the lethal cases will be reported rapidly. The
occurrence of morbidity in non-endemic areas, as well as the lack of dead rodents, should be
the first signs to consider an intentionally caused plague epidemic [19].
Brucella species are Gram-negative coccobacilli or short rods. Three major human pathogens
cause the zoonotic infection brucellosis—B. melitensis, B. abortus, and B. suis. The source and
reservoir of the bacteria are sick animals—goats, sheep, cows, pigs, and dogs. Main transmis-
sion routes are contact, erogenic, and alimentary (foodborne). After an incubation period of
1–6 weeks, nonspecific symptoms such as fatigue, fever, sweating, and muscle pain occur.
Enlarged lymph nodes and liver are frequently found. Arthritis, meningitis, encephalitis,
pyelitis, and so on may develop in severe forms. Some signs and symptoms may persist for
longer periods of time.
3.4. Enterobacteria
The genus Salmonella is part of the family Enterobacteriaceae and consists of rod-shaped, Gram-
negative, flagellated facultative anaerobes.
Salmonellae are divided into two categories: invasive typhoidal serotypes causing typhoid
fever and non-typhoidal Salmonella causing salmonellosis [21].
Unlike typhoidal salmonellae (Salmonella Typhi and Salmonella Paratyphi), where humans are
the only recognized reservoir, the main reservoir of non-typhoidal Salmonella is the intestinal
tract of different domestic animals which often results in the contamination of foodstuffs [22].
Salmonella is predominantly found in eggs, poultry, dairy products, fresh fruits, and veg-
etables [23].
Gastrointestinal symptoms usually start 4–72 h after the ingestion of contaminated food or
water and last for 4–7 days. They include fever, chills, nausea, vomiting, abdominal cramping,
and diarrhea. Diarrhea is usually self-limiting and may be grossly and bloody. After the onset
of the disease, salmonellae are excreted in feces for approximately 5 weeks.
Although salmonellosis is regarded as a relatively mild disease, severe illness and death can
occur in some cases—particularly in infants, elderly, and immuno-compromised patients
[24]. Bacteremia appears in 5–10% of infected persons and in some cases may progress to
focal infection, such as meningitis, bone, and joint infection [25].
https://www.facebook.com/myfreefoodindustrybooks/
Salmonella infections generally do not require treatment. A correct rehydration is the most
important, while antibiotics are prescribed only in severe cases.
The safety measures for the prevention of Salmonella infection include washing hands before
food processing and especially after handling raw meats; cooking meat, and eggs thoroughly;
avoiding consumption of foods containing raw eggs or milk; and avoiding direct contact
between uncooked meat with food that will not be cooked.
As Salmonella spp. are readily available and have the potential to cause outbreaks with mod-
erate morbidity, but with significant effects on public health, they are included in group B
of possible biological agents (Table 1). Organizations or individuals with limited biological
knowledge and laboratory access can easily use them for bioterrorist purposes, as in the case
of the biggest bioterrorist attack in the USA (see the Introduction, section [7]).
Bacteria of the genus Shigella are a common cause of bacterial diarrhea worldwide, especially
in developing countries. There are four different species: Shigella dysenteriae (serogroup A),
Shigella flexneri (serogroup B), Shigella boydii (serogroup C), and Shigella sonnei (serogroup D)
[26]. Shigellae are Gram-negative, non-motile, and facultative anaerobic pathogens [27].
Humans are the only reservoirs for these bacteria and the disease is transmitted person to
person by the fecal-oral route.
Shigella is highly contagious and 10–100 bacteria can initiate infection when sanitation or per-
sonal hygiene is poor. Patients at the highest risk for disease are young children in daycare
centers, refugee camps, and nurseries [28].
Shigella, unlike Vibrio cholerae and most Salmonella species, is acid resistant and survives pas-
sage through the stomach to reach the intestine. Shigellae attach to, invade, and replicate in
the mucosal epithelium of the distal ileum and colon, causing inflammation and ulceration
[28]. Shigella infection is generally limited to the intestinal mucosa, and bacteremia due to
Shigella is rare.
S. dysenteriae produces a (Shiga) toxin, which can cause damage to the intestinal epithelium
and glomerular endothelial cells, the latter leading to kidney failure [28].
Shigellosis is characterized by fever, abdominal pain, and watery diarrhea with traces of
blood and pus. The disease is usually self-limiting but may become life threatening if patients
are immuno-compromised or if adequate medical care is not available. The treatment consists
of oral rehydration and antibiotics administration [29].
Shigella may be released through the deliberate contamination of food or water supplies dur-
ing a hypothetical terrorist attack. Secondary transmission can result from exposure to the
stool of infected individuals because the diarrheal fluids are highly infectious.
To prevent the spread of bacteria, appropriate sanitation measures should be taken: sewage
disposal and water chlorination, insect control, handwashing, and proper cooking of food [28].
https://www.facebook.com/myfreefoodindustrybooks/
Escherichia coli is the most common and important member of the genus Escherichia. This
organism is a Gram-negative, rod-shaped, facultative anaerobic bacterium. Most E. coli strains
are part of the normal intestinal flora of healthy humans and animals. However, there are
some strains associated with a variety of diseases, including gastroenteritis, urinary tract
infections, and meningitis. Among them, enterohemorrhagic E. coli (EHEC) are defined as
pathogenic E. coli strains that produce Shiga toxins and can cause severe illness such as hemor-
rhagic colitis and the life-threatening sequelae hemolytic uremic syndrome, characterized by
hemolytic anemia, thrombocytopenia, and renal injury. E. coli O157:H7 was first recognized
as a pathogen in 1982 during an outbreak investigation of hemorrhagic colitis in Oregon and
Michigan, the USA [30]. This E. coli O157:H7 outbreak was linked to under-cooked ground
beef hamburgers and cheeseburgers sold from a fast-food restaurant chain. The most frequent
route of transmission for E. coli O157:H7 is via the consumption of contaminated food and
water Raw or undercooked meat, unpasteurized dairy products, and fruit juices have been
frequently implicated in reported outbreaks [31]. In addition, E. coli can also spread directly
from person to person, particularly in child day-care units. E coli O157:H7 has a low infec-
tious dose and resists in the environment for more than 10 months [32]. A potential airborne
transmission has also been reported [33].
The essential factor of E. coli O157:H7 pathogenesis is the production of Shiga toxins (Stx-1,
Stx-2, or both), which disrupt protein synthesis of the host. Stx-1 is identical to the Shiga toxin
I produced by Shigella dysenteriae, while Stx-2 is more toxic [32].
The diseases caused by EHEC ranges from mild, uncomplicated diarrhea to hemorrhagic coli-
tis with severe cramping (abdominal pain) and bloody diarrhea. The incubation time is from
3 to 4 days. Occasionally vomiting occurs in approximately half of the patients. Fever is either
low grade or absent. The illness lasts for 4–10 days and is usually self-limited.
All people are susceptible to hemorrhagic colitis, but young children and the elderly are
affected more seriously. In a terrorist attack, E. coli would most likely spread via food and
water contamination. Secondary transmission can result from exposure to the stool of already
infected patients, as diarrheal fluids are highly infectious. The period of infectivity of stool is
typically a week or less in adults but 3 weeks in one-third of children.
Patients can be protected with standard sanitation precautions and handwashing is of par-
ticular importance. For uncomplicated cases, rehydration is the only treatment needed. Fluid
and electrolyte replacement is important when diarrhea is watery or there are signs of dehy-
dration. Antibiotics are often avoided in E. coli O157:H7 infections since some evidence sug-
gests that antibiotic treatment may lead to complications.
Currently, no vaccine is available to prevent E. coli O157:H7 infections.
Staphylococcus aureus is the second leading cause of gastroenteritis in the world (after salmo-
nellosis) [34]. Its food-poisoning property is due to the production of staphylococcal entero-
toxins preformed in the food.
https://www.facebook.com/myfreefoodindustrybooks/
Staphylococcus aureus is found on the skin, mammary glands, nose, and throat of about 25% of
healthy people [36]. So, the personnel in restaurants can be a significant source of contamina-
tion, as one of the typical ways of infection spread is the contact-alimentary route.
The prophylactics of staphylococcal food poisoning is done by using proper hygiene and
sanitation measures when preparing food. The most critical are handwashing with soap or
alcohol; wearing gloves; fast cooling; and fridge storage of prepared food [37].
Staphylococcal toxins could be successfully used as a biological weapon by both food con-
tamination or aerosolization. In this context, enterotoxin B, which may cause fever, cough,
difficulty in breathing, headache, vomiting, and nausea, is the most promising [36]. It is stable
and water soluble, can be easily aerosolized, but however is rarely lethal [38]. Only higher
exposure to the toxin could lead to septic shock and death in some people.
The gas gangrene is an acute, severe wound infection with a highly invasive character.
Bacteria propagate in the traumatized tissue (muscles) and produce a variety of toxins. The
most important is the α-toxin (lecithinase), which destroys the cell membranes, including
those of the erythrocytes, and leads to hemolysis. The enzymatic activity is responsible for
gas release in the infected tissues. Clinically, the infection manifests as pain, edema, cellulitis,
and necrosis in the wound area. The mortality rate is relatively high. Laboratory diagnosis
consists of anaerobic cultivation and biochemical tests. Penicillin G is the preferred antibiotic,
but more important is the chirurgical treatment of the wound.
The incubation period of the foodborne infection is 8–16 h and the disease is characterized by
watery diarrhea, cramps, and vomiting. Usually, it gets resolved in 12–24 h and the treatment
is predominantly symptomatic [40].
https://www.facebook.com/myfreefoodindustrybooks/
Clostridium perfringens produces at least 12 toxins and one or more of them can be used as a
biological weapon. The neurotoxin epsilon is the most promising as biological agent [9]. It is
found in zoonotic C. perfringens type B and D [38]. The zoonosis represents as rapid toxemia
usually in sheep but also in goat and cattle. The ingested spores germinate rapidly, propagate,
and produce a non-active protoxin of 311 amino acids. After an intestinal proteolysis, a potent
and lethal necrotizing toxin is synthetized. It enters the blood stream and causes kidney dam-
age and pulmonary edema [41]. The toxin also has extreme neurotropism which results in
serious neurological injury [42].
Knowledge about the effect of the toxin on humans is not available—all data are obtained
from animal experiments. However, one can speculate that to produce a significant impact on
the society, the aerosolic form of the toxin should be used [43].
V. choleraе, V. parahaemolyticus, and V. vulnificus are the most important species responsible
for food poisoning among the Gram-negative, comma-shaped bacteria from the genus Vibrio.
Three types of V. choleraе are known: type 01, type 0139, and type non-01 [44]. Type 01 is typically
linked with classic cholera (biotypes Inaba, Ogawa, Hykoschima and El Tor), while type 0139
can cause cholera-like illness and atypical infections. These bacteria are found in sea and ocean
coastal waters. Approximately two-thirds of V. choleraе food poisoning is linked to the consump-
tion of raw or not sufficiently heat-treated sea products. The vibrios easily survive under 10°C
and multiply fast under temperatures of 30–37°C with a generation time of 12–18 min in raw
seafood. Vibrio species can divide in an alkaline environment and under the high concentration
of NaCl (up to 10%) but cannot resist high temperatures (>70°C) and dehydration.
Vibrios of type 01 cause classic cholera, which is transmitted usually by drinking water but also
with contaminated food and human contacts. The incubation period is relatively short—from
6 h to 5 days—and the most typical symptom is the watery diarrhea with profuse, “rice-water”
stool. The massive water and electrolyte loss, as well as the severe intoxication, is due to the
cholera toxin, produced during the intestine colonization. The diarrhea lasts for 6–7 days and in
the cases of cholera gravis, which results in severe dehydration, up to 60% of patients can die.
V. рarahaemolyticus usually causes milder cholera-like infections [45] and only 3% of all strains
are pathogenic and responsible for acute gastroenteritis. Typical symptoms are nausea, vomit-
ing, stomach aches, sub-febrile temperature, and watery or watery-bloody diarrhea. The incu-
bation period is 12–96 h after the consumption of contaminated food or water and the disease
lasts up to several days but in rare cases, it can extend to 10 days with septicemia and host death.
V. vulnificus is associated with wound infections after a contact with contaminated seawater
or sea animal species. It causes septicemia with a lethality of approximately 50% and rarely
induces gastroenteritis in individuals with liver damage.
The treatment of cholera requires urgent, adequate, and well-timed rehydration. Usually, oral
rehydration with low osmolarity or cereal-based solution and, when necessary, replacement
of intravenous fluids and electrolytes are sufficient to reduce the lethal cases to 1% of all
infected patients [46, 47]. In addition, zinc supplementation can reduce the duration and the
severity of diarrhea in children with cholera [48]. Antibiotics, although a secondary measure,
https://www.facebook.com/myfreefoodindustrybooks/
also help, as they limit the duration of the disease. They are recommended in moderately and
severely ill patients, but their choice should be determined by the local antibiotic sensitivity
patterns. Doxycycline is recommended as a first-line treatment for adults, while azithromycin
is recommended for children and pregnant women [36].
As cholera is a typical water- and foodborne infection the prophylaxis is associated with high
personal hygiene and sanitation measures. Bottled, boiled, or treated water should be used
for drinking and food preparing in endemic areas or during outbreaks. Any seafood should
also be freshly cooked and served hot. Vaccination, although not generally recommended, is
useful for travelers to areas of active cholera transmission.
Because Vibrio cholerae is a waterborne bacterium, the most likely bioterrorism use will be
via contaminated water and/or food. In 1961, China alleged that cholera has been used as a
weapon in Hong Kong by the US army. In 1969, Egypt also alleged the “imperialistic aggres-
sors” of using cholera in Iraq in 1966 [49]. However, due to the regular chemical treatment
of public water supplies (at least in the developed countries), it will be difficult to cause а
high-scale damage.
4. Conclusion
Conflict of interest
Authors declare the absence of any conflict of interest related to this work.
Author details
References
[1] Bedros JR, Szoboszlay S, Kriszt B. Bioterrorism – Are we ready to face it? In the shadow
of facts and presumptions part 2: Blasting microbes*. AARMS Terrorism. 2005;4(1):63-81
[2] Kortepeter MG, Parker GW. Potential biological weapons threats. Emerging Infectious
Diseases. 1999;5(4):523-527
[3] Harris S. Japanese biological warfare research on humans: A case study of microbiology
and ethics. Annals of the New York Academy of Sciences. 1992 Dec 31;666:21-52
[4] Sotos JG. Botulinum toxin in biowarfare. Journal of the American Medical Association.
2001 Jun 6;285(21):2716
[5] Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, et al.
Botulinum toxin as a biological weapon: Medical and public health management.
Journal of the American Medical Association. 2001 Feb 28;285(8):1059-1070
[6] Zilinskas RA. Iraq’s Biological Weapons. The Past as Future? JAMA. 1997 Aug
6;278(5):418-424
[7] Török TJ, Tauxe RV, Wise RP, Livengood JR, Sokolow R, Mauvais S, et al. A large com-
munity outbreak of salmonellosis caused by intentional contamination of restaurant
salad bars. Journal of the American Medical Association. 1997 Aug 6;278(5):389-395
[8] Kolavic SA, Kimura A, Simons SL, Slutsker L, Barth S, Haley CE. An outbreak of Shigella
dysenteriae type 2 among laboratory workers due to intentional food contamination.
Journal of the American Medical Association. 1997 Aug 6;278(5):396-398
[9] CDC. CDC | Bioterrorism Agents/Diseases (by category) | Emergency Preparedness
& Response [Internet]. 2017 [cited 2018 Jan 8]. Available from: https://emergency.
cdc.gov/agent/agentlist-category.asp
[10] Peck MW. Biology and genomic analysis of clostridium botulinum. Advances in
Microbial Physiology. 2009;55:183-320
[15] Laudisoit A, Ruppitsch W, Stoeger A, Pietzka A. Yersinia pestis: Plague. In: BSL3 and
BSL4 Agents. Weinheim, Germany: Wiley-VCH Verlag GmbH & Co. KGaA; 2012.
pp. 312-7
https://www.facebook.com/myfreefoodindustrybooks/
[16] Perry RD, Fetherston JD. Yersinia pestis--etiologic agent of plague. Clinical Microbiology
Reviews. 1997 Jan;10(1):35-66
[17] Cunha BA. Anthrax, tularemia, plague, ebola or smallpox as agents of bioterrorism:
Recognition in the emergency room. Clinical Microbiology and Infection. 2002
Aug;8(8):489-503
[18] Butler T. Plague into the 21st century. Clinical Infectious Diseases. 2009 Sep 1;49(5):736-742
[19] Riedel S. Plague: From natural disease to bioterrorism. Proceedings (Baylor University.
Medical Center). 2005 Apr;18(2):116-124
[20] Gul ST, Khan A. Epidemiology and epizootology of brucellosis: A review. Pakistan
Veterinary Journal. 2007;27(3):145-151
[21] Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-
typhoidal salmonella disease: An emerging and neglected tropical disease in Africa.
Lancet. 2012;379(9835):2489-2499
[22] Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis: The role of poultry meat. Clinical
Microbiology and Infection. 2016;22(2):110-121
[23] Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH. Salmonella: A review
on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Sciences.
2015;8(3):284-293
[25] Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid salmonella infection: Microbiology, clin-
ical features, and antimicrobial therapy. Pediatrics and Neonatology. 2013;54(3):147-152
[26] Joh RI, Hoekstra RM, Barzilay EJ, Bowen A, Mintz ED, Weiss H, et al. Dynamics
of shigellosis epidemics: Estimating individual-level transmission and reporting
rates from national epidemiologic data sets. American Journal of Epidemiology.
2013;178(8):1319-1326
[27] Killackey SA, Sorbara MT, Girardin SE. Cellular aspects of Shigella pathogenesis:
Focus on the manipulation of host cell processes. Frontiers in Cellular and Infection
Microbiology. 2016;6(March):1-11
[28] Ryan K, Ray CG, editors. Sherris Medical Microbiology: An Introduction to Infectious
Disease. 4th ed. New York: McGraw-Hill; 2004
[29] Schroeder GN, Hilbi H. Molecular pathogenesis of Shigella spp.: Controlling host cell
signaling, invasion, and death by type III secretion. Clinical Microbiology Reviews.
2008;21(1):134-156
[30] Rangel JM, Sparling PH, Crowe C, Griffin PM, Swerdlow DL. Epidemiology of
Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerging Infectious
Diseases. 2005;11(4)
https://www.facebook.com/myfreefoodindustrybooks/
[31] Neil KP, Biggerstaff G, MacDonald JK, Trees E, Medus C, Musser KA, et al. A novel vehi-
cle for transmission of Escherichia coli O157:H7 to humans: Multistate outbreak of E. Coli
O157:H7 infections associated with consumption of ready-to-bake commercial prepack-
aged cookie dough-United States, 2009. Clinical Infectious Diseases. 2012;54(4):511-518
[32] Lim JY, Yoon J, Hovde CJ. A brief overview of Escherichia coli O157:H7 and its plasmid
O157. Journal of Microbiology and Biotechnology. 2010;20(1):5-14
[33] Varma JK, Greene KD, Reller ME, DeLong SM, Trottier J, Nowicki SF, et al. An outbreak
of Escherichia coli O157 infection following exposure to a contaminated building. Journal
of the American Medical Association. 2003;290(20):2709-2712
[34] Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Genetics and
Molecular Research. 2003;2(1):63-76
[36] Centers for Disease Control and Prevention. Staphylococcal Food Poisoning | Food
Safety | CDC [Internet]. 2016 [cited 2018 Jan 10]. Available from: https://www.cdc.gov/
foodsafety/diseases/staphylococcal.html
[37] Lalla F, Dingle P. The efficacy of cleaning products on food industry surfaces. Journal of
Environmental Health. 2004 Sep;67(2):17-22
[38] Clarke SC. Bacteria as potential tools in bioterrorism, with an emphasis on bacterial
toxins. British Journal of Biomedical Science. 2005;62(1):40-46
[39] Petit L, Gibert M, Popoff MR. Clostridium perfringens: Toxinotype and genotype. Trends
in Microbiology. 1999 Mar;7(3):104-110
[40] Freedman JC, Shrestha A, McClane BA. Clostridium perfringens enterotoxin: Action,
genetics, and translational applications. Toxins (Basel). 2016 Mar 16;8(3)
[41] Greenfield RA, Brown BR, Hutchins JB, Iandolo JJ, Jackson R, Slater LN, et al.
Microbiological, biological, and chemical weapons of warfare and terrorism. The
American Journal of the Medical Sciences. 2002 Jun;323(6):326-340
[42] Finnie JW. Pathogenesis of brain damage produced in sheep by Clostridium perfringens
type D epsilon toxin: A review. Australian Veterinary Journal. 2003 Apr;81(4):219-221
[43] Pappas G, Panagopoulou P, Christou L, Akritidis N. Category B potential bioterrorism
agents: Bacteria, viruses, toxins, and foodborne and waterborne pathogens. Infectious
Disease Clinics of North America. 2006 Jun;20(2):395-421
[44] Kaper JB, Morris JG, Levine MM, Levine MM. Cholera. Clinical Microbiology Reviews.
1995 Jan;8(1):48-86
[45] Broberg CA, Calder TJ, Orth K. Vibrio parahaemolyticus cell biology and pathogenicity
determinants. Microbes and Infection. 2011 Nov;13(12-13):992-1001
https://www.facebook.com/myfreefoodindustrybooks/
[46] Daniels NA, Simons SL, Rodrigues A, Gunnlaugsson G, Forster TS, Wells JG, et al. First
do no harm: Making oral rehydration solution safer in a cholera epidemic. The American
Journal of Tropical Medicine and Hygiene. 1999 Jun;60(6):1051-1055
[47] World Health Organization. WHO Position Paper on Oral Rehydration Salts to Reduce
Mortality from Cholera; 2008
[48] Roy SK, Hossain MJ, Khatun W, Chakraborty B, Chowdhury S, Begum A, et al. Zinc
supplementation in children with cholera in Bangladesh: Randomised controlled trial.
British Medical Journal. 2008 Feb 2;336(7638):266-268