Content uploaded by Ewen Cameron David Todd
Author content
All content in this area was uploaded by Ewen Cameron David Todd on Jan 16, 2016
Content may be subject to copyright.
Trends in Foodborne Disease
Ewen C. D. Todd
Food Safety Policy Center, Michigan State University, East Lansing, Michigan USA.
Abstract
Foodborne disease is widespread around the world with its most serious consequences on
those who are young, old and already-ill. Chemical contaminants are present in much of
the food supply but usually at levels not associated with adverse human effects. However,
there are occasional problems from natural toxins that can cause local disease and restrict
international trade. Much of food monitoring is focused on testing foods to meet the
national standards for mycotoxins and pesticide residues. More recently, there have been
concerns over specific chemicals like acrylamide, food dyes and melamine as well as
allergens, but there is no routine testing for these. Despite this concern over chemicals
and their monitoring, most of the known illness relate to microbial contamination, and
surveillance systems that link to human illness. Interestingly, many foods that have been
associated with outbreaks would not have been thought of as vehicles from the then-
existing microbiological studies, e.g., Salmonella in chocolate and peanut butter; E. coli
O157:H7 in apple cider and sprouts; Listeria monocytogenes in hot dogs. Many steps
have to be taken to bring a foodborne disease outbreak investigation to a successful
conclusion. As is so often the case, if key data are missing or the different players in the
investigation do not coordinate effectively, not only will many ill persons not be
identified, but the cause of the outbreak may not be determined. Surveillance can be
comprised of two main systems: complaint or notification systems, and pathogen-specific
surveillance. The former may trigger an investigation and the latter leads to interpretation
of case trends over periods of time. More recently there has been interest in syndromic
surveillance as a way of rapidly detecting an event even if the causative agent may not
yet been identified. Most countries have some kind of disease surveillance system and
these usually include enteric diseases but not necessarily foodborne disease per se. Those
countries that do tend to have their own approach to surveillance which is mainly passive
in letting the local investigators prepare the reports and communicate these to national
levels. An important step in foodborne disease surveillance is the development and
maintenance of an active system, like FoodNet and PulseNet in the USA, even if it is
time-consuming and expensive. This is because they can be very useful in predicting the
burden of foodborne disease at the national level and what the main risk factors are that
lead to infections, which in turn help direct control measures. A new concern today is the
threat of deliberate contamination of food, and early disease detection systems that link to
first responders are being developed. In preparation for such an event, not only do public
health personnel need to be involved, but also law enforcement officers who have a
different mandate. This threat is stimulating better traceability methods particularly for
imported foods, and having governments and industry being more concerned over fraud,
counterfeiting and smuggling. Eventually, foodborne disease surveillance systems will
become integrated internationally, as they are starting to do within Europe and under the
direction of the World Health Organization. The ultimate goal of all food safety programs
is to prevent contaminated products from reaching the consumer. The World Health
Organization indicates that although the global incidence of foodborne disease is difficult
to estimate, in 2005 alone an estimated 1.8 million people died from diarrheal diseases
(WHO, 2007). A great proportion of these cases can be attributed to contamination of
food and drinking water. Additionally, diarrhea is a major cause of malnutrition in infants
and young children. In historical times, and today in many countries, most food was
locally obtained and quickly eaten. Cooking would reduce the likelihood of pathogens
being present and spoilage was avoided for longer-term storage through fermentation,
drying, or cooling. Today, we rely on much more complex food supply chains that
increase the number of potential points of contamination and opportunities for microbial
growth from farm to table. Most of the common agents causing foodborne disease are
zoonotic in origin, i.e., transmitted from animals to humans. Examples are
Campylobacter from poultry, E. coli O157:H7 and BSE prions from cattle, and Yersinia
enterocolitica from swine. Most of the pathogens of concern to us do not cause illness in
these animals but are means of transmission to ourselves. They carry them in their
gastrointestinal tracts, from where they spread to other animals, inadequately composted
animal manure, and to water. After slaughter and processing, there is a risk that small
amounts of fecal matter are left on the meat surfaces. Intensified animal production, in
which cattle, pigs and chickens are kept at high densities, increases the risk of transfer of
pathogens between animals and, thus more animal products are likely to be contaminated.
In addition, some pathogens are widely dispersed in nature and are present in many wild
animals, such as Salmonella in insects, birds, reptiles and mammals, and Giardia in
beavers. Other pathogens come from human sources either directly through person-to-
person contact or through contamination of food by water or sewage; these include
Shigella, Staphylococcus aureus, hepatitis A virus and norovirus (Greig et al., 2007;
Todd et al., 2007 b, c).
Environmental contaminants of microbial origin are rarer in developed countries but they
can be present in low amounts. These include mycotoxins such as patulin in apple juice,
aflatoxin in cottonseed and peanuts, and deoyxnivalenol (vomitoxin) in winter wheat.
There are standards for these toxins that limit trade, since sometimes it is difficult to grow
crops without some fungal growth, especially in tropical places like Africa, but they are
set at levels well below the threshold of harmful chronic effects (Bullerman, 2003). More
likely to cause acute intoxications are aquatic toxins from seasonal algal blooms such as
paralytic shellfish poison in clams, diarrhetic shellfish poison in mussels, and ciguatoxin
in tropical fish; countries tend to have monitoring programs for these and restrict sales
when a limit is reached. All these toxins are resistant to normal cooking temperatures,
and therefore have to be avoided rather than destroyed. Under conditions of drought
stress, unseasonal rains, or high moisture, before or harvest, can allow the proliferation of
molds like Fusarium, Aspergillus or Claviceps to produce T-2 toxin, aflatoxins or ergot,
respectively, in quantities if consumed that would cause severe illnesses or death. These
have occurred in the past where starvation conditions necessitated consuming the
contaminated crops, or there was improper harvesting of grain which was baked into
bread (ref).
2
Foodborne disease covers many areas but is primarily thought of in terms of infectious or
toxigenic agents causing acute illnesses. Some anthropogenic chemical agents found in
foods are regulated because of their possible link to chronic disease but this has been
largely based on animal studies and are mostly hard to substantiate with human data.
However, it is known that persistent organic pollutants (POPs) can accumulate in human
and animal tissue through longterm exposure. The most common of these pollutants are
the chlorinated hydrocarbons mainly found in a number of pesticides used in agriculture,
homes and industry; the polychlorinated biphenyl (PCBs) and PCB-oxidation by products
like dioxins and furans; and the heavy metals. The pollutants enter the food chains of
food animals mainly due to anthropogenic activities like fossil fuel burning, vehicle
exhausts, waste incineration, metalliferous mining and smelting, agricultural chemicals,
inorganic fertilizers and liquid and solid waste from animals and humans. The 2001
Stockholm POPs treaty will require the banning all production of POPs with limited
country-specific and general exceptions once at least 50 countries agree (EPA, 2007).
Pesticide residues are normally well controlled in foods produced in developed countries,
but there are recent concerns with some chemicals. It is uncertain whether we should or
are able to regulate the potential carcinogen acrylamide, identified as a compound
produced during cooking in 2002, with potato chips, French fries, bread and coffee being
the more commonly implicated foods (DiNovi, 2006). The highest levels found so far are
in starchy foods (potato and cereal products). Acrylamide has always been present in our
food supply and although it is possible to reduce it, elimination from our present diet is
impossible. This is opposed to the recall of hundreds of brands of foods in many
countries containing Sudan dye in 2005. The reason that Sudan I dye is banned in these
countries is that it can contribute to an increased risk of cancer through animal studies,
but the likelihood of human illness arising from the dye at the levels present in these
foods is very low. Since July 2003, cargoes of dried and crushed or ground chili and
curry powders coming into any EU Member State have to be accompanied by a
certificate showing they have been tested and found to be free of Sudan I. Any
consignment that does not have a certificate must be detained for sampling and analysis
(FSA, 2007). Most recently melamine, an unapproved chemical added to pet food to
enhance nitrogen content, and its analog cyanuric acid, caused concern in early 2007, not
only because of deaths of dogs and cats in Canada and the US, but also because of the
apparent lack of control in exporting countries and the high demand for cheap food or
ingredients from importing nations. However, based on a worst case scenario, if
melamine and cyanuric acid were present in equal amounts in all the solid food consumed
by an individual every day, the potential exposure is about 250 times lower than the level
considered safe. This is a large safety margin (USDA, 2007).
Surveillance systems for foodborne disease vary in capacity by country. Generally, the
more developed the country is, the more funding that is put into its surveillance
programs, but no country has an outstanding system that could serve as a model for all
others. An additional problem is lack of consistency. Approaches to surveillance and
available resources change over time, so that apparent trends may reflect more the
changes the way the data are collected and processed. Another problem is the lack of
coordination in surveillance systems between most countries, so that information can be
3
rapidly and efficiently shared, although efforts are being made to have common
denominators in some areas, like pulse net gel electrophoresis profiles (PulseNet) and
Enter-Net (now Global-Net) for Salmonella and other enteric pathogens. Nevertheless,
over many decades we have learned much from foodborne disease surveillance on how
disease agents are transmitted through the food supply, and where contamination and
growth by pathogens in the food production and preparation chain typically occur.
Without past experience, we would never have suspected foods such as chocolate, peanut
butter, sprouts, spinach, carrot juice, tahini, basil or raspberries to have caused major
outbreaks. Two factors are driving better surveillance today: the increasing demand for
imported products to meet seasonal and exotic expectations by consumers, and the threat
of deliberate contamination by terrorists or those bearing a grudge against a food
operation. In addition, many countries are starting to set goals for reduction of disease
within their borders through science-based policies. Attempts are also being made to
create regional surveillance networks in different parts of the world, initiated by
organizations like WHO and PAHO. In addition, the Internet is being increasingly used
to enhance infectious disease surveillance and outbreak investigation. A survey in 2004
of state and local communicable disease investigators responsible for infectious disease
surveillance and outbreak investigation in three states showed that the majority (70.7%)
of the 297 respondents accessed the Internet for information regarding infectious disease
surveillance and outbreaks at least weekly (M'ikanatha et al. (2006).
The broad objective of foodborne and enteric disease surveillance systems has been
defined to identify disease causes so that prevention and control programs can be
introduced and strengthened (Todd, 2001). There are several elements in a
well-designed surveillance system.
1. Early alert of illnesses or potential illness to prevent further spread of disease.
2. Notification of enteric or other specific diseases that are often foodborne
through physicians reporting to a central epidemiological agency and reports of
laboratory isolations of enteric pathogens to a reference laboratory.
3. Investigation of incidents of foodborne illness and reporting of results on a
regular basis.
4. The use of sentinel and special epidemiological studies to determine a more
realistic level of morbidity of a foodborne disease. Because of the limitations of
the passive reporting system, sentinel studies are considered as one approach to
discover the extent of a foodborne disease in a community, the information
from which can be extrapolated to a region or country.
5. Estimation of health and economic impacts and setting directions for control
programs. A foodborne disease surveillance system can also be used to
estimate the health and economic impacts of foodborne diseases including
cost-benefit risk-benefit studies, to anticipate problems and focus research into
areas of high risk, to evaluate the effectiveness of current preventive and
control practices, and to provide information upon which to base goals and
priorities for food-safety programs.
6. Monitoring of animals, crops, foods and their ingredients for the presence of
pathogens, chemicals and allergens.
4
Most countries have some passive system that allows data on foodborne illnesses to be
sent to centralized authorities where summaries are generated. However, these depend on
the uneven quality of the source data that vary according to the resources allocated at the
local level. Active surveillance systems collect data targeted to answer specific
epidemiological questions more efficiently, but at such a high cost that most countries do
not have the resources, except on a occasional basis. There is also the issue of what to do
with the collected data. There has to be a conscious effort to translate the problems
identified from the surveillance programs to consider strategies for prevention and
control of foodborne disease. Otherwise, there is little value in having these kinds of
monitoring programs.
Thus, we can consider surveillance as a) identifying human disease related to food
consumption; and b) detecting contaminants that may have an adverse effect on human
health in the food supply from farm to fork. Both of these lead to potential prevention and
control strategies to reduce the likelihood of acute or chronic disease. Most food
containing pathogens or chemicals does not have easily-distinguished markers for the
consumer, like a distinctive smell, taste or color change. Food samples are normally
selected for testing either because they have implicated in an outbreak, have been
involved with contamination issues in the past, or are under a regulatory testing scheme.
It is impractical to monitor the whole food supply for possible contaminants. However,
even in samples suspected of causing illness or involved in recalls, pathogens and to a
lesser extent chemicals are not evenly distributed in the food source. Thus, sampling can
be time-consuming and expensive both for industry and government. Although the US
does not have a comprehensive program for monitoring live food animals, unlike some
EU countries, various US food safety agencies test for pathogen prevalence in certain
foods through routine monitoring and case studies. FSIS monitoring, focused on the
slaughter process, includes regular testing of raw meat and poultry for salmonellae,
ground beef for E. coli O157:H7, ready-to-eat deli products for multiple pathogens, and
FSIS and the Agricultural Research Service examine pathogen prevalence in commercial
food products, such as L. monocytogenes in frankfurters (Batz et al., 2005). The
government’s commitment to monitoring for pathogens at low levels is illustrated by
FSIS’ tests ground beef every year for E. coli O157:H7. This is because it is classed as an
adulterant in the US and has been linked to many cases of foodborne illness outbreaks.
Yet, positive detections in thousands of samples are very low. There are approximately
1,400 federally inspected establishments producing raw ground beef, the raw products
that are currently routinely sampled for E. coli O157:H7 as part of the Agency's HACCP
verification programs. From 2001 to 2006 the percent positives ranged from >0.87 (2001)
to 0.17 (2005) with up to over 10,000 samples taken every year (FSIS, 2007). Not only is
prevalence of pathogens rare but also concentrations (levels) of organisms in foods
implicated in illness are often low. This is illustrated by the 245 reported cases in England
in 1982 resulting from the sale of 600,000 chocolate bars imported from Italy with a very
low dose of an average value of 1.6 Salmonella Napoli cfu/g per bar and a likely
infective dose of 50 organisms (Greenwood and Hooper, 1983). In another large
international chocolate-associated Salmonella outbreak originating from Germany that
affected 439 laboratory-confirmed cases in 7 European countries and Canada over 10
5
months, estimates of the number of S. Oranienburg cfu/g ranged from 1.1–2.8, sufficient
to cause a 29% hospitalization rate (Werber et al., 2005). In 1996, in one of the largest
outbreaks in US history with 593 confirmed cases and an estimated 224,000 cases of
salmonellosis were traced to ice cream containing <6 cfu per serving (Hennesey et
al., 1996). One reason for these low doses (and in other outbreak examples) are these
foods facilitate protection of the organism in its passage through the stomach to the
intestines, mainly through the presence of fat. This same food matrix tends also to
preserve the organisms for subsequent analysis. Salmonella have been recovered
from chocolate after many months or even years (Werber et al., 2005). Even more
astonishing is the E. coli O157:H7 outbreak in Japan where 6,000 cases were linked
to consumption of imported radish sprouts but the pathogen was not found in any of
the sprouts tested (Michino et al., 1999).
In 2005, the EU's rapid alert system received a total of 947 notifications from regulators
on aflatoxins (Anonymous, 2006), mainly for pistachio nuts, primarily originating from
Iran. Aflatoxins were also regularly reported in peanuts and derived products (219
notifications) originating from China, Brazil, Argentina and Ghana. Within the group of
nuts and nut products, 64 notifications concern hazelnuts and derived products
originating from Turkey and Azerbaijan. Notifications were also made for almonds and
derived products (originating mainly from the US), for dried figs and derived products
(Turkey), melon seeds (Nigeria), chili, paprika, curry and nutmeg (India, Turkey and
Pakistan). Between 1996 and 1998, 580 liters of milk in Mexico were surveyed for
aflatoxin B (Carvajal et al., 2003). Pasteurization and ultrapasteurization of milk did not
control the aflatoxin contamination, which was present in 13% of samples at ≥0.05
μg/liter and in 8% at ≥0.5 μg/liter. The milk on the market with least aflatoxin was
imported milk powder with vegetable oil.
Foodborne disease outbreak surveillance also has limitations to detect an incident. Even
in a large outbreak, the time interval between a contamination event and an alert and
public recall of incriminated food may be considerable, as illustrated by the E. coli
O157:H7 spinach outbreak in the US in 2006 (Todd et al., 2007a) and many earlier
outbreaks. The sequence typically requires many steps depending on the extent of the
outbreak and whether the infecting agent is one routinely tested or not. Each of steps
requires a period of time to progress through: (1) the initial exposure to a contaminant in
a food (ingestion); (2) the incubation period that can range from hours to weeks; (3)
presentation of the sick individual to a medical facility, and/or a complaint to a local
health department; (4) recording of the complainant information by the department and
taking action to proceed further; (5) collection of a clinical specimen by a nurse/physician
and shipping it to a public health laboratory (a private laboratory may not report results to
anyone but the requester); (6) simultaneous initiation of outbreak or sporadic case
investigation by the local health department; (7) diagnostic laboratory testing finds a
positive result and informs the physician and the responsible health agency; (8) interview
of patients if a larger event (2 or more cases) is suspected, leading to a full outbreak
investigation, (9) further laboratory characterization of the isolate(s), such as serotype,
phage type or molecular biotype, and reporting to public health authorities; (10) sharing
information with other laboratories and epidemiologists at the state/provincial level to
6
identify a regional outbreak; (11) recognition of a large outbreak requiring national
assistance, e.g., CDC; (12) analysis of all available epidemiological and laboratory
surveillance data, (13) possible initiation of a case-control study; 14) food identified with
a likely regional or national recall, (15) national public reporting; and (16) a publication
of the outbreak on public record. From this it can be seen that, detection and investigation
of outbreaks can be a lengthy process, and sometimes it is not successful in determining
the agent, the vehicle, or the specific risk factors. Even in the well-investigated E. coli
spinach outbreak the precise means of contamination were not determined (California
Food Emergency Response Team, 2007; Todd et al., 2007a). As can be seen from this
lengthy sequence of events, usually cases in outbreaks cannot be prevented by public
health action unless there is a continual source of food that can be recalled and destroyed
(one contaminated meal for a social event is long gone, and perishable items like lettuce,
spinach and sprouts have a limited shelf life, compared with more shelf-stable products
like hard cheese or chocolate bars with a much longer marketable sales period).
Nevertheless, outbreak investigation and reporting even with its limitations has revealed
unanticipated problems that can have control measures applied to prevent similar future
events. National and even international historic surveillance data are proving useful for
public health policies including developing risk assessments, determining food
attribution, and assessing total burden of foodborne illness. A comparison of the different
issues involved in monitoring of food and surveillance of foodborne disease is shown in
Table 1. Most of these have been discussed above.
7
Table 1. Comparison of Food Monitoring and Disease Surveillance1
Food Monitoring Disease Surveillance
Prevention potential Prevention of later outbreak cases
possible
Secondary prevention only
(some outbreaks are
investigated early enough
that cases are prevented by
removal the contaminated
source)
Speed of pathogen detection Potentially fast for screening but
up to 5 days (or occasionally
longer) for culture
Fast, if pathogen is the
dominant organism
Sampling Issues
Denominator (United States) >356 billion lbs food/year 300 million people
Sample selection By risk or control point Self-selection
Agent distribution in sample Uneven Generally homogenous
Contamination introduction
points
Many in the food chain Ingestion through mouth
Testing Issues
Pathogen load Generally low in foods Generally high in clinical
specimens
Matrices containing pathogens Complex, varied, sometimes
difficult to culture from
Predictable, few, easier to
culture
Injured cells Common Not common unless
antibiotics are used
Pathogen persistence Can persist for long periods of
time (e.g., refrigerated, fermented,
dried, low aW products)
Stool: limited to
colonization period in
intestines; vomitus usually
early at illness site
Inhibitory substances to
pathogen survival
Frequent as food constituents or
additives
Rare
Predictive value of broad
surveillance (monitoring)
Low for whole commodities High for specific
populations
Cost of broad surveillance
(monitoring): many samples
tested to find a positive
Very high Relatively low
1Modified from Besser (2006).
8
Besser (2006) suggests the three most common approaches to foodborne disease
surveillance approaches are: 1) complaint or notification systems; 2) pathogen-specific
surveillance; and 3) syndromic surveillance. These differ in their application and
limitations although they do not need to be mutually exclusive (Table 2). Consumer
complaints are investigated by environmental health officers (sanitarians) and notification
systems depend on the physician requesting a laboratory specimen to be tested, and/or
noting a common event from the patients they see whether in a clinic or hospital. Because
of the large number of these local operations or activities, the quality and resources vary
considerably. Complaints relating to food safety have also been documented at the US
national level with the Consumer Complaint Monitoring System (CCMS), of the Food
Safety and Inspection Service (FSIS) of the USDA. This has assisted public health
agencies with evaluating consumer about 4,000 complaints through phone calls on a
hotline since January 2001 (Elenberg and Dubrawski, 2006). Complaints typically
involve reports of illness, injury, foreign objects, contamination (including chemical
contamination), allergic reactions, and improper labeling. However, the system has
recognized several outbreaks of Salmonella, Listeria monocytogenes, and E. coli
O157:H7. Unlike the complaint or notification systems, the pathogen-specific
surveillance systems tend to use relatively few large laboratories using standardized
methodologies for testing and typing clinical specimens or monitoring food samples.
However, it is often the complaints that lead to a recognition of a cluster that is confirmed
by the pathogen-specific surveillance system. The laboratory-based systems are mainly at
state/provincial and national levels, but they also have international connections, as
demonstrated by the WHO Global Salm-Surv for training and expertize in foodborne
disease, initiated in 2000. World Health Organization Global Salm-Surv is a collaborative
effort between WHO, the Danish Institute for Food and Veterinary Research, the United
States Centers for Disease Control and Prevention, Reseau International Des Instituts
Pasteur, Health Canada, the Animal Sciences Group, The Netherlands, the United States
Food and Drug Administration, Enter-net - human enteric pathogen surveillance network,
Europe, and OzFoodNet - Enhanced Food borne Disease Surveillance Network, Australia
(WHO, 2004). The program is aimed at reducing foodborne diseases worldwide through
enhancement of laboratory-based surveillance and outbreak detection and response.
Through this program, collaboration and communication between epidemiologists and
microbiologists nationally and internationally, involved in human disease, animal disease,
and food safety, is fostered. The network now has almost 900 members (including
national institutions, as well as individual experts) from 141 countries (WHO, 2006).
Enter-Net funded by the European Commission is a EU-based network for Salmonella
and all verotoxigenic E. coli (VTEC), not limited to E. coli O157:H7 (EU, 2002a). Enter-
Net continued to strengthen global surveillance of these infections through collaboration
with WHO and non-EU countries, including EU-candidate countries, Canada, the United
States, South Africa, Japan and Australia. Its use is demonstrated in the Salmonella
Oranienburg chocolate outbreak, described in detail below. Today, however, Enter-Net
has been transferred to the European Centre for Disease Prevention and Control (ECDC,
2007), which became operational in 2005, and called Global-Net. The centre’s tasks
include: 1) Enhancing the capacity of the Community and the Member States individually
to protect human health through the prevention and control of human disease; 2) acting
on its own initiative when outbreaks of contagious illnesses of unknown origin are
9
threatening the Community; and 3) Ensuring complementary and coherent action in the
field of public health by bridging together the tasks and the responsibilities of the
Member States, the EU Institutions and the relevant International Organizations.
The European Food Safety Authority was established in 2002 by regulation EC178/2002,
which laid out the general principals of food law and decreed that risk assessment and risk
management should be conducted separately (Halliday, 2007). At that time, consumer confidence in food safety
structures was at a low, after the BSE crisis of the 1990s. In its five years of operation, EFSA has
conducted 55 peer reviews and continues to respond to BSE, dioxin and Salmonella issues, but
also has input on emerging technologies such as nanotechnology and cloning, and nutrition-related public health
issues like obesity.
Data from the US demonstrates the way passive and active surveillance systems are used.
The passive Foodborne Disease Outbreak Surveillance System, managed by the Centers
for Disease Control and Prevention (CDC), is designed to investigate foodborne
outbreaks and establish both short-term control measures and long-term improvements to
prevent similar outbreaks in the future (CDC, 2005). The CDC defines an outbreak as
two or more people who were ill after eating the same food. Olsen et al., (2000) reported
on outbreaks from 1993 to 1997. During this period, a total of 2,751 outbreaks of
foodborne disease were reported (489 in 1993, 653 in 1994, 628 in 1995, 477 in 1996,
and 504 in 1997).
In September 2000, states began receiving federal funding to plan and implement
integrated electronic systems for disease surveillance which resulted in improved
reporting (MMWR, 2005). Today, CDC and the US states use the Electronic Foodborne
Outbreak Reporting System (eFORS) to record and report their information, with data in
many states transmitted on a secure, Internet-based, communicable disease reporting
system. This improvement should aid in more consistence approaches to sharing data and
the timeliness of response to disease outbreaks at local, state, and national levels.
However, Scripps News studied 6,374 food-related disease outbreaks reported by every
state to the CDC from Jan. 1, 2000, through Dec. 31, 2004 (Hargrove, 2006). The causes
of nearly two-thirds of the outbreaks in that period were officially listed as "unknown."
State and local epidemiologists diagnosed an average of just 36 percent of the nation's
reported outbreaks even though some outbreaks had hundreds of cases. Although a few
states appeared to have a good surveillance and diagnosis record, many reported
surprisingly few cases of pathogens like E. coli O157:H7. Thus, the passive system
underestimates the burden of foodborne disease, even though the specific details on the
outbreaks that are investigated are very useful for prevention and control purposes. An
example of this is the studies reported by Greig et al (2007) and Todd et al (2007b, c) to
look at outbreaks originating from food workers, mainly from the US but also from
Canada and other parts of the world over many years. There seemed to be no decrease in
these type of outbreaks over several decades, although the type of dominant pathogen
changed (from Salmonella to norovirus). By analyzing the risk factors and how these
outbreaks originated, pointers to control strategies were suggested.
The Foodborne Disease Active Surveillance Network (FoodNet) is able to generate more
specific foodborne disease information than the passive system about numbers of cases
and risk factors. FoodNet, a collaboration of CDC, the USFDA, and the USDA, was
10
created in 1996 to conduct population-based, active surveillance for foodborne infections.
The primary objectives of FoodNet are to: 1) determine the epidemiology of bacterial,
parasitic, and viral foodbome diseases; 2) determine the prevalence of foodborne diseases
in the United States; and 3) investigate the link between certain foods and the proportion
of foodborne disease caused by their ingestion. FoodNet conducts surveillance for E. coli
O157:H7, Campylobacter, Listeria, Salmonella, Shigella, Yersinia, Vibrio,
Cryptosporidium, and Cyclospora. This has been successful in monitoring, tracking
trends, and defining risk factors for causes of foodborne illnesses, and in estimating the
burden of foodborne illnesses in the United States (CDC, 2002a). With the availability of
FoodNet to generate more specific foodborne disease information, Mead et al. (1999)
estimated that 76 million cases, 325,000 hospitalizations and 5,000 deaths occur each
year in the US. Of these, only 14 million are attributed to known agents; the other 62
million are of unknown origin. Thus, even though this estimate is accepted as the best to
date, there is a high degree of uncertainty as to what is causing many foodborne illnesses.
These estimates indicate that three pathogens, Salmonella, Listeria, and Toxoplasma, are
responsible for 1,500 deaths each year, Norwalk-like viruses account for over 67% of all
cases, 33% of hospitalizations, and 7% of deaths. However, researchers stressed that the
assumptions underlying the Norwalk-like viruses figures are among the most difficult to
verify (Mead et al., 1999). Other important causes of severe illness are Salmonella and
Campylobacter, accounting for 26% and 17% of hospitalizations, respectively.
PulseNet USA is a national molecular surveillance network of local public health
laboratories that performs characterization (DNA fingerprinting) of pathogens that may
be foodborne to identify outbreaks in a timely manner. The network permits rapid
comparison of the different DNA profiles on the web through an electronic database at
the CDC. The PulseNet system is currently used to track nine diseases by use of
standardized PFGE protocols. Since its inception in 1996, it has been instrumental in the
detection, investigation and control of numerous outbreaks caused by Shiga toxin-
producing Escherichia coli O157, Salmonella, Listeria monocytogenes, Shigella spp., and
Campylobacter (Gerner-Smidt et al., 2006). This dramatically lowered the number of
reported cases needed to detect widespread outbreaks. In 1997, PulseNet enabled the
Colorado Department of Health to detect an outbreak caused by potentially contaminated
beef that led to the recall of 25,000,000 pounds of beef, and 18,600,000 pounds in 2002
(CDC, 2002b). Another good example is the 2003 outbreak of vacuum-packed blade-
tenderized steaks, which was initially detected by two cases with unique PFGE subtypes
and resulted in the recall of 739,000 pounds of potentially contaminated product
distributed in multiple states (Laine et al., 2005). An outbreak of Salmonella Kiambu
associated with beef jerky in 2003 was detected by linking PFGE patterns from food
monitoring to disease surveillance patterns, resulting in the recall of 22,000 pounds of
contaminated product (Smelser, 2004, Besser, 2006). PulseNet systems are used in other
countries and one example of this is demonstrated in the S. Oranienburg outbreak
originating from German chocolate (Werber et al., 2005). Despite the arsenal of tools
available for investigating enteric illnesses, large multistate outbreaks still take time for
investigation and reporting as indicated by the E. coli O157:H7 in spinach (205 cases,
11
California Food Emergency Response Team, 2007; Todd et al, 2007a) and lettuce (71
cases, CDC, 2006) outbreaks in 2006, and the Salmonella in peanut butter episode in
2007 (628 cases, MMWR, 2007a).
12
Table 2. Comparison of enteric disease surveillance approaches
Complaint/Notificatio
n
Pathogen-
specific
Surveillance
Syndromic
Surveillance
(nonspecific health
data)
Timeliness after
first indication
of illness
Fast follow-up if resources
allow
Relatively
slow
Fast
Sensitivity of
cluster detection
Intermediate, best with
local clusters ill at the
same time
High if
samples or
specimens
available
Low unless there is a
relatively large event
Types of enteric
agents
Typical or unusual Standard
agents under
surveillance
only
Typical or unusual
Strengths Detection of local
outbreaks
Detection of
widespread
outbreaks
Detection of large, local
or regional outbreaks,
does not depend on lab
analysis
Modified after Besser (2006)
Syndromic surveillance
Syndromic surveillance is the third type of disease surveillance that could potentially be
applied to detection of problems in the food supply. Syndromic surveillance has been
used for early detection of outbreaks, to follow the size, spread, and tempo of outbreaks,
to monitor disease trends, and to provide reassurance that an outbreak has not occurred
(Henning, 2004). Syndromic surveillance systems seek to use existing health data in real
time to provide immediate analysis and feedback to those charged with investigation and
follow-up of potential outbreaks. The apparent benefits of syndromic surveillance include
potential timeliness, increased response capacity, ability to establish baseline disease
burdens, and ability to delineate the geographical reach of an outbreak (Berger et al.,
2006). Potential outbreaks are detected by spikes in the incidence of common syndromes
or surrogate indicators rather than agent or personal recognition, so in theory these
systems should be able to detect problems due to known or unknown agents. However,
optimal syndrome definitions for continuous monitoring and specific data sources best
suited to outbreak surveillance for enteric diseases have not been determined. The
primary problem with syndromic surveillance is an unfavorable signal-to-noise ratio. The
number of cases needed to trigger the system is inversely proportional to the specificity
(Besser, 2006). Thus, syndromic surveillance based on nonspecific health data is useful
for detecting very large local events but is very insensitive to small or widespread events.
Broadly applicable signal-detection methodologies and response protocols that would
maximize detection while preserving scant resources are being sought. Syndromic
surveillance is unlikely to detect an individual case of a particular illness. Typically, a
13
program for gastroenteritis could look at surveillance of stool submissions at clinical
laboratories, over-the-counter (OTC) pharmacy sales for antidiarrheal agents, and
possibly for diarrheal illness at certain sites like nursing homes, schools or hospitals.
Several large networks have been established to conduct syndromic surveillance in the
US, such as BioSense, the Electronic Surveillance System for Early Notification of
Community-based Epidemics (ESSENCE), and National Retail Data Monitor (NRDM)
(Burkom et al., 2004). Real Outbreak Detection System (RODS) has been used for
foodborne outbreak surveillance in some states. Based on a simulated inhalational
anthrax after an aerosol release, the earliest detection using a temporal algorithm was 2
days later (Buckeridge et al., 2005). Earlier detection tended to occur when more persons
were infected, and performance worsened as the proportion of persons seeking care in the
prodromal disease state declined. From this we can deduce that a massive foodborne
attack would also take time to detect. However, the cases in the above scenario would
seek medical care, whereas in a foodborne outbreak there may also be calls to local health
departments complaining about food items.
Two examples of early warning systems for communicable diseases to complement the
routine surveillance system indicate strengths and weaknesses of syndromic surveillance.
Data relating to 10 key syndromes (primarily respiratory and gastrointestinal) were
received electronically from 23 call centers covering England and Wales during
December 2001 to February 2003 (Cooper et al., 2004). Data were analyzed daily and
statistically significant excesses, termed exceedances, in calls were automatically
highlighted and assessed by a multidisciplinary team. When the surveillance team
determined that information provided by line listings necessitated further investigation,
the team generated an alert by passing call information to the relevant local or national
public health teams for follow-up. A total of 1,811 exceedances occurred, of which 126
required further investigation and 16 resulted in alerts to local or national health-
protection teams. There were 14 exceedances and 4 alerts for diarrhea and 28
exceedances and 4 alerts for vomiting. The surveillance is continuing daily for the entire
population of England and Wales. The ALERT system in the Republic of Serbia with 11
targeted syndromes showed the mixed results to be expected from such a syndromic
surveillance system (Valenciano et al., 2004). ALERT triggered timely investigation and
control of outbreaks of hantavirus and salmonellosis. For instance, an increase in cases of
acute watery diarrhea was confirmed to be salmonellosis in one district and control
actions were launched. In contrast, ALERT failed to detect clusters of brucellosis and
tularemia targeted by the 'unexplained fever' syndrome. Those clusters were detected by
the routine surveillance system through hospital notification, weeks or months after their
occurrence. In a retrospective study of medical records following a major waterborne E.
coli O157:H7 outbreak in Ontario, Canada in 2000, the number of cases could have been
reduced from the 1346 documented because of earlier detection of persons with bloody
diarrhea in local area hospitals (Davies et al., 2006).
Although interest in syndromic surveillance has increased because of concerns about
bioterrorism, it should not be implemented at the expense of traditional disease
surveillance, and should not be relied upon as a principal outbreak detection tool. It has
yet to be seen as a part of routine surveillance activities in most countries. One area that it
14
can be effective is to monitor large events over many days like the Olympics or the
World Cup. For instance, the 2003 Rugby World Cup provided an opportunity to test the
viability of a near real-time syndromic surveillance system in metropolitan Sydney,
Australia (Muscatello et al., 2005). Information captured for each emergency department
(ED) visit included patient demographic details, presenting problem and nursing
assessment entered as free-text at triage time, physician-assigned provisional diagnosis
codes, and status at departure from the ED. Both diagnoses from the EDs and triage text
were used to assign 26 syndrome categories. The system did not identify any major
public health threats associated with the event, mass gatherings or the influx of visitors.
However, it demonstrated the feasibility and potential utility of syndromic surveillance
using routinely collected data from ED information systems. This system had no impact
on clinical staff, with its use of statistical methods to assign syndrome categories based
on clinical free text information. The syndromic surveillance monitoring at this Rugby
World Cup with multiple venues in a large city indicates that any serious illnesses would
quickly be recognized and some degree of containment instituted. This study indicates
that a similar monitoring system could be in place for any large public event in other
countries where food was deliberately or accidentally contaminated, and if imported food
was implicated, specific quarantine measures be brought into play.
Surveillance in developing countries
Developing countries tend to have weaknesses in their government public health systems
that fail to ensure adequate consumer protection and also weaken their trading abilities
for exported food (FAO, 2002). Such weaknesses include:
•Outdated food laws, standards and regulations, and sometimes overregulation;
•No centralized approach, or even coordination among departments and agencies,
to food control with jurisdictional confusion and overlap;
•Lack of adequately trained personnel to carry out compliance activities, including
food inspection;
•Limited capacity in terms of physical structure, equipment, supplies and technical
personnel of food control laboratories, where they exist;
•The inability of food industries (preharvest, processing, retail, foodservice) to
consistently follow good hygienic practices (GHP), good manufacturing practices
(GMP) and the hazard analysis critical control point (HACCP) systems, even if
they are familiar with these concepts because they do not have the technical
ability, or will, to do so;
•The inability of government and food industries of many developing nations to be
able to compete effectively in the export market by being in compliance with the
dominant food quality and safety agreements (most notably the Agreement on the
Application of Sanitary and Phytosanitary Measures (SPS) of the Codex
Alimentarius Commission;
15
•Conflict between public health objectives and facilitation of trade and industry
development; and
•Limited opportunities for appropriate scientific inputs in decision-making
processes.
Many of these countries may not be able to overcome not only these weaknesses but the
resources sufficient to maintain a national foodborne disease surveillance system,
although this should be a long-term goal. For instance, there could be targeted surveys of
high risk products that have been implicated in outbreaks in the past, finding consumer
opinions of on their perception of the safety of the food supply, and even regional
cooperation among neighboring countries for setting up programs like PulseNet.
Policy uses of surveillance data
The US is one of the few countries to attempt to set goals for a quantitative reduction of
foodborne disease. Such goals are to be found in all agencies in the US working to
reduce foodborne disease to achieve public health goals as outlined in the Healthy People
2010 initiative (Healthy People 2010, 2006). More than a dozen federal agencies share
the lead in articulating and implementing a wide variety of health related goals. The
primary foodborne goal is to reduce by 50% the incidence of disease from the main
foodborne diseases over the period 1997-2010. Goals are close to being on target for
Campylobacter, E. coli O157:H7, and Listeria monocytogenes, but progress has generally
remained static over the last few years despite industry and government new initiatives,
indicating that there are some barriers that have to be identified and overcome. Also,
there has been little improvement in salmonellosis where the rate in 2006 was
14.8/100,000, far short of the 2010 goal of 6.8 (MMWR, 2007b). The rate for HUS in
children <10 years, as a surrogate for serious E. coli infections, 1.63/100,000 vs. the goal
of 0.9.
Risk assessments have also relied on surveillance data to supply pathogen profiles or
hazard identification data. A risk analysis conducted by the U.S. Department of
Agriculture on E. coli O157:H7 in U.S. slaughterhouses, for example, showed that the
overall level of risk was driven by the preharvest load of E. coli. The analysis also
showed that a combination of intervention procedures would be more effective than any
one intervention in reducing contamination (Todd and Narrod, 2006). In addition, case
estimates have been used to “anchor” those ill, as in the FDA/FSIS/CDC quantitative
assessment of relative risk to public health from foodborne Listeria monocytogenes
among ready-to-eat foods (2003).
Another area where data on foodborne illnesses are proving useful is food attribution to
help prioritize effective food safety interventions. This is the capacity to attribute cases of
foodborne disease to the food vehicle or other source responsible for illness (Batz et al,
2005). A wide variety of food attribution approaches and data are being used in different
countries, such as Denmark, UK and the US. Surveillance data including the analysis of
outbreaks, case-control studies, microbial subtyping and source tracking methods, and
expert judgment, are all being considered. For instance of the estimated 61,000 E. coli
16
O157:H7 cases associated with food (Mead et al., 1999), how many of these cases are
attributed to which foods, such as ground beef, salami, sprouts, lettuce, spinach, soft
cheese, raw milk, etc? The initial step is to group food vehicles into suitable large
categories such as poultry, eggs, pork, beef, dairy, fish, shellfish, wild game, row crops,
and tree crops. Each of these commodities could be divided further, leading to such
subcategories. One of the difficult issues is whether or not to class foods with multiple
ingredients, such as soups or pizzas, by their main ingredient, proportionally by the
contributing ingredients, or leave this group of foods out of the analysis altogether. A
common food categorization scheme is essential if different sources of data are to be
combined or compared, with acceptability to industry, academia, and consumer groups
(Batz et al., 2005). Expert elicitation is another way of generating attribution and other
data for determining risk and priorities, when scientific or epidemiologic data are lacking,
sparse, or highly uncertain. Expert elicitations are, however, limited because they are
based on perception, not on observable data, and circular or biased reasoning can
contribute to the final analysis unless carefully screened out.
Outbreak scenario
An international outbreak of Salmonella Oranienburg illustrates the strengths and
weaknesses of a large outbreak investigation and implementation of control measures
(Werber et al., 2005). In mid-October 2001, the National Reference Center for
Salmonella and Other Enteric Pathogens (NRC) in Hamburg noted an unusual increase in
the number of S. Oranienburg isolates received in October. On November 19, the NRC
informed the federal health department that it had received a S. Oranienburg isolate in
September. The isolate was submitted by a private laboratory for serotyping and had
come with the additional source information "confectionery sample". Upon inquiry, a
large German chocolate manufacturer, which produced a broad variety of chocolates
called the federal health department on November 27, and confirmed that it had sent in
the confectionery sample. The positive sample originated from an in-house control of a
chocolate product and the pertaining batch, due to be exported to the United States, was
completely destroyed and not distributed. Nevertheless, the number of S. Oranienburg
notifications had sharply increased and continued to rise. A standard exploratory
questionnaire was distributed on November 20, 2001 through state health departments to
all local health departments to aid the collection of data on food and environmental
exposure from cases. In addition, local health departments were asked to immediately
interview patients with newly reported S. Oranienburg infections about chocolate
consumption in the seven days before disease onset, and also to send any remaining
chocolate to a food safety laboratory. A case-patient was defined as a person with
gastroenteritis starting after October 1, 2001 who had been reported with a S.
Oranienburg infection to a public health department before December 6. Cases, however,
continued after December and into March, 2002 with a total ill of 439 persons, who had a
median age of 15 years. On December 11, one day after the Enter-net request was
distributed, Denmark was the first country to respond but other countries did supply
information as well, with food histories and microbiological results from S. Oranienburg
patients in several other countries pointing to the same source.
17
Results of the preliminary analysis of a case control study were available on December
14. Three variables relating to the seven-day period prior to symptom onset of the case-
patient were significantly associated with disease: 1) having shopped at the same food
chain; 2) having consumed this chain’s chocolate; 3) having eaten (any kind of) chocolate
on a daily basis. Thus, S. Oranienburg infection was significantly associated with the
consumption of chocolate from one chain that had obtained it from a single manufacturer
in the week prior to symptom onset, but not in the seven days before the interview. Case-
patients were more likely than control subjects to report eating chocolate daily, likely
indicating an increased probability of exposure to contaminated chocolate.
For comparison by the use of PFGE, S. Oranienburg isolated from stool specimens were
sent to the NRC from laboratories in Germany and, on Enter-net request, from other
countries. In addition, isolates from chocolates were submitted from state or private food
laboratories in Germany as well as from Canada and the Czech Republic. Furthermore,
patient isolates from the outbreak period shared a PFGE profile with isolates from
chocolates but differed from isolates of patients who became sporadically diseased with
S. Oranienburg before the outbreak. The PFGE profiles of S. Oranienburg isolates from
patients with symptom onset after October 1, 2001 (outbreak period) in Germany and in
the 5 other European countries, except Canada, were indistinguishable, but differed from
S. Oranienburg isolates from German patients with symptom onset before October. The
Canadian cases therefore were not a part of this outbreak but occurred from another
unidentified source, as did cases in Germany earlier than October 1. All the chocolate
isolates showed PFGE profiles indistinguishable from human isolates of the outbreak
period.
Beginning December 11, a nationwide chocolate sampling of German chocolates in
grocery stores was initiated. On December 18, the finding of S. Oranienburg in a
chocolate leftover of a patient led to an immediate public warning and recall of all
chocolates of this brand with specific production numbers. The recall was extended to
other products from the same company a few days later. Chocolates included in the
German recall were promptly withdrawn from the market in other European countries as
well as in Canada. In Canada, Finland, and Sweden, samples from withdrawn chocolates
tested positive for S. Oranienburg. Overall, S. Oranienburg was found in 18 (5%) of 381
chocolates that were tested and reported to federal health department during the outbreak
period. S. Oranienburg was isolated from two different brands from the same
manufacturer; all positive chocolates were produced during the same week in August
2001. Estimates of the number of Salmonella in the tested chocolates ranged between 1.1
and 2.8 cfu/g. The local food safety authority in Germany did not identify hygienic
deficiencies at the production facility, and samples obtained in the beginning of
December 2001 from in-house chocolates, cocoa and cocoa powder from a supplier of the
chocolate manufacturer tested negative. Nothing from the August production week was
available for testing.
Five main conclusions were reached.
1) The protracted nature of chocolate-associated outbreaks probably reflects both the long
shelf-life of chocolate and the long survival of Salmonella in these products. S.
Oranienburg was isolated from chocolates five months after manufacture, and Salmonella
18
survived even longer in a S. Napoli outbreak in England and Wales, where this interval
was 12 months.
2) Multinational collaboration facilitated by Enter-net helped in preventing contaminated
chocolate from entering the market in Canada, Finland and Sweden, thereby averting
human illness. Furthermore, by rapid electronic exchange and comparison of PFGE
profiles, the Canadian cluster of human cases could be classified as unrelated to this
outbreak.
3) In this outbreak, it remains unclear whether the salmonellae survived the heating or
contaminated the chocolate afterwards. Consequently, long-term preventive measures to
render chocolate production safer could not be implemented.
4) An Enter-net urgent inquiry was sent after the first results of molecular subtyping
suggested a link between human cases and this chocolate. Until then, investigators in
Germany and Denmark had worked independently unaware that the outbreak extended
outside of their respective countries. An earlier inquiry, ideally as early as an outbreak
was suspected by the investigating countries, may have speeded the up the investigation
to have helped identify the vehicle earlier, thereby preventing further cases.
5) Finally, a public warning or recall of the chocolate products did not occur before
leftovers tested positive although the results of the case-control study, the Danish
investigations (which pinpointed the specific chocolate brand earlier than the German
investigation because in Germany there were many German brands on the market), and
the subtyping comparison between human isolates and the original submitted in-house
sample in November had clearly indicated that this manufacturer’s products as the source
of the outbreak. Yet, because no specific product or lot had been identified at the time, a
recall or a public warning were considered excessive responses by the German food
safety authority. However, it is quite possible that leftover or dated products may not
yield an agent either because of die off of the pathogen over many months, or it was not
present in those specific samples because of erratic contamination of the product.
Traceability
Traceability is the ability of a company, a retail chain or an industry sector to trace the
history of a product from production and distribution to consumption or use in another
product. The need for traceability comes from two directions: logistics and safety.
Traceability is a key component for reducing risks of microbial and chemical
contamination by reviewing the production, harvesting and production practices in the
information recorded through the tracking system. Also, if a deliberate attack were
planned, limiting its effect or spread should be facilitated by rapidly identifying the
source through such a system. An increasing demand by consumers for safe and high
quality food has led governments, agricultural production operations, and food industries
to explore ways of maintaining control of products. The use of barcodes, radio frequency
identification (RFID) chips, and time-temperature indicators (TTI) are increasingly used
19
to track product through the food chain and also monitor temperature and humidity
changes, along with leak indicators to detect changes in modified gas atmospheres and
biosensors to detect pathogens. Traceability systems also assist in traceback investigations
of outbreaks. Tracebacks follow the contaminated food product backwards along the food chain
to identify the possible source(s) of the contamination, and if the labeling of the product is robust
enough, investigators can quickly reach back to the source of the contamination. In the E. coli
spinach outbreak of 2006, the traceback investigation implicated four fields on four different
ranches as the source of contamination (California Food Emergency Response Team, 2007).
While E. coli bacteria were found on all the ranches, only one of the ranches had the outbreak
strain of E. coli O157:H7. Although this investigation was not fast or complete, without some
kind of tracking system, the source farm would never have been found. If traceability is a
necessary part of food safety, how should it be regulated? In Europe traceability is
mandatory from farm to fork as of January 2005 (EU, 2002), while in the US this is not
yet the case and is the responsibility of the businesses. However, with the recent case of
BSE in the US and the possible threat of bioterrorism or avian flu, some are arguing for
more effective traceability policies in the global food supply chain. Thus, there is a link
between surveillance and traceability. Tracking systems are increasingly able to monitor
food through its production and delivery to retail, and lessen the likelihood that these will
cause illness or contain high numbers of microorganisms and other contaminants.
Fraud, counterfeiting and smuggling
Although these activities have always occurred within the food production and selling
system, it does not usually surface at the consumer level. The Jungle by Upton Sinclair
published in 1906 was an early example of the scandals in the meat industry because of
unhygienic slaughtering and packaging processes by companies, with unapproved items
being sold as edible food products. Although the BSE crisis in the UK did not arise
because of fraudulent practices, the public was surprised and in some cases disgusted that
ruminant cattle would be fed meat and bone leftovers. Because of the BSE incidents in
the 1990s starting in the UK and spreading to other parts of Europe and the world, and
subsequent consumer and government concern, labeling was introduced in the European
beef sector requiring specific information on the origin of the meat in 2002. However,
later inspections showed that a substantial proportion of beef products did not comply
with the labeling requirements (Verdenius, 2006). This is borne out by the discovery of a
company in Northern Ireland illegally exported beef during the embargo resulting from
the BSE crisis in the late 1990s, to French vendors, who then sold it on the market
between 1996 and 1998 (Johnston, 2007). Invoices seized at that time prove that there
was a clear violation of the embargo imposed on beef products and was done knowingly
and illegally. In a more recent fraud case, two directors of Euro Freeze, a cold storage
company in Northern Ireland were sent to jail in June 2007 for 4 months each for
breaching Ireland's food safety laws with 36 charges relating to the illegal use of a
veterinary control label, and with tampering with documents related to a consignment of
beef cheek meat (ElAmin, 2007). Intensified official veterinary controls on warehouses
supplying Chinese retailers resulted in the seizure of smuggled poultry products in Italy,
and low pathogenic strains (LPAI) was found in lung and trachea from both frozen duck
and chicken carcasses (Beato et al., 2006). Thus, criminal activities for economic gain
also may pose an increasing food safety risk as products from around the world can enter
20
the food system of any country. The recent concern over imported Chinese food products
with antibiotics and melamine emphasize this point. Better surveillance means fewer
smuggled items but current spot check methods for imports will not catch many of these
illegal entries.
Conclusions
Surveillance of foodborne disease is an ongoing issue dependent on good science and
available resources, both economic and personnel. Surveillance has to be able to integrate
the different epidemiological and laboratory components especially in a federated system
with multiple jurisdictions. This means that some countries are going to be able to
develop their surveillance programs to keep up with both the newest scientific advances
and also with the ever-changing threats, both naturally occurring and deliberate. But other
nations, particularly developing countries, will lag behind. This makes a global system
difficult to manage. However, in today’s world, food is available from all corners of the
earth and the varieties of products including value-added items is bewilderingly large.
This makes monitoring of imported and domestic foods by testing almost impossible.
This has led to the HACCP concept where the producers have to demonstrate their
understanding of the production and processing of their food, what the greatest risks are,
and how to monitor the critical control points. Recent food scares and outbreaks show
that this does not always work. This is partly because of poor management planning and
worker error. However, some of the outbreaks have been from foods and situations that
have not been considered risky in the past, e.g., sprouts, peanut butter, spinach, and new
control measures have to be considered to respond to these. This is where surveillance is
critical to at least understand the reasons that outbreaks occur, so that regulatory
programs and educational strategies can be implemented.
21
References
Anonymous. 2006. FoodNavigatorEurope.com. Special alfatoxin measures target repeat
offenders. 15/9/2006 - http://www.foodnavigator.com/news-by-product/news.asp?
id=70601&idCat=94&k=aflatoxin-imports-pistachios. Accessed July 3, 2007.
Batz, M. B., Doyle, M. P., Morris, Jr., J. G., Painter, J., Singh, R., Tauxe, R.V., Taylor,
M.R., and Lo Fo Wong, D. M. A. 2005. Attributing illness to food. Emerg. Infect. Dis.
11 (7): 993-999. Available from http://www.cdc.gov/ncidod/EID/vol11no07/04-
0634.htm. Accessed July 5 2007.
Beato, M.S., C. Terregino, G. Cattoli, and I. Capua. 2006. Isolation and characterization
of an H10N7 avian influenza virus from poultry carcasses smuggled from China into
Italy. Avian Pathol. 35(5): 400-403.
Berger, M., Shiau, R., and ,Weintraub, J. M. 2006. Review of syndromic surveillance:
implications for waterborne disease detection. J. Epidemiol. Commun. Health 60(6): 543-
550.
Besser, J. 2006. Surveillance of the food supply. In Addressing Foodborne Threats to
Health: Policies, Practices, and Global Coordination, Workshop Summary. Board on
Global Health. 177-189. http://books.nap.edu/openbook.php?
record_id=11745&page=177. Accessed June 27, 2007.
Buckeridge D. L., Switzer, P., Owens, D., Siegrist, D., Pavlin, J., and Musen, M. 2005.
An evaluation model for syndromic surveillance: assessing the performance of a temporal
algorithm. MMWR 54 Suppl: 109-115.
Bullerman, L.B. 2003. Mycotoxins. In Encyclopedia of Food Sciences and Nutrition. 2nd
edit. B. Caballero, L.C. Trugo and P.M Finglas, eds Academic Press, New York. pp.
4080-4086.
Burkom, H. S., Elbert, Y., Feldman, A., Lin, J. 2004. Role of data aggregation in
biosurveillance detection strategies with applications from ESSENCE. MMWR 53 Suppl:
67-73.
California Food Emergency Response Team. 2007. Investigation of an Escherichia coli
O157:H7 outbreak associated with dole pre-packaged spinach. Final March 21, 2007.
California Dept. of Health Services, Sacramento, CA, and the US Food and Drug
Admin., Almeda, CA. http://www.dhs.ca.gov/ps/fdb/local/PDF/2006%20Spinach
%20Report%20Final%20redacted.PDF. Accessed June 29, 2007.
Carvajal, M., Rojo, F. Méndez, I., and Bolañosy, A. 2003. Aflatoxin B1 and its
interconverting metabolite aflatoxicol in milk: the situation in Mexico. Food Additives
and Contaminants 20 (11): 1077–1086.
22
CDC. 2002a. Centers for Disease Control and Prevention. Preliminary FoodNet data on
the incidence of foodborne illnesses --- Selected Sites, United States, 2001. MMWR 51:
325-329.
CDC, 2002. Multistate outbreak of Escherichia coli O157:H7 infections associated with
eating ground beef—United States, June-July 2002. MMWR 51(29): 637–639.
CDC. 2005. Centers for Disease Control and Prevention. Foodborne Disease Outbreak
Surveillance System. http://www.cdc.gov/foodborneoutbreaks/index.htm. Accessed July
5, 2007.
CDC. 2006. Multistate outbreak of E. coli O157 infections, November-December 2006.
Updated December 14, 2006. http://www.cdc.gov/ecoli/2006/december/121406.htm.
Accessed June 29, 2007.
Cooper DL; Smith G; Baker M; Chinemana F; Verlander N; Gerard E; Hollyoak V;
Griffiths R. 2004. National symptom surveillance using calls to a telephone health advice
service--United Kingdom, December 2001-February 2003. MMWR 53 Suppl:179-183.
Davies, R. F. and ECADS Partners and Collaborators. 2006. Detection of Walkerton
gastroenteritis outbreak using syndromic surveillance of emergency room records. Adv.
Dis. Surveill. 1:20.
DiNovi, M. 2006. The 2006 Exposure assessment for acrylamide. CFSAN/Office of Plant
& Dairy Foods, Food and Drug Administration, Washington D.C.
http://www.cfsan.fda.gov/~dms/acryexpo.html. Accessed July 3, 2007.
ECDC. 2007. European Centre for Disease Prevention and Control, Stockholm, Sweden.
http://europa.eu/agencies/community_agencies/ecdc/index_en.htm. Accessed November
20, 2007.
ElAmin, A. 2007. Directors of Irish food company sentenced to jail. June 8. FoodProduction Daily.
http://www.foodproductiondaily.com/news/ng.asp?n=77216-euro-freeze-fsa-d-arcy.
Accessed June 8, 2007.
Elenberg, K., and Artur Dubrawski, A. 2006. The consumer complaint monitoring
system: enhancing discovery and mitigation of foodborne threats to health through
pattern surveillance and multiple-attribute algorithms. In Addressing Foodborne Threats
to Health: Policies, Practices, and Global Coordination, Workshop Summary. Board on
Global Health. 189-194. http://books.nap.edu/openbook.php?
record_id=11745&page=189. Accessed June 27, 2007.
EPA. 2007. Persistent Organic Pollutants (POPs).
http://www.epa.gov/oppfead1/international/pops.htm. Accessed November 21, 2007.
23
EU. 2002a. International surveillance network for the enteric infections -Salmonella and
VTEC O157. European Commission – DG SANCO. Agreement No SI2.326441
(2001CVG4 – 021) Enter-net – Human enteric pathogen surveillance Network.
http://ec.europa.eu/health/ph_projects/2000/com_diseases/fp_commdis_2000_inter_01_e
n.pdf. Accessed July 2, 2007.
EU. 2002b. Regulation (EC) No. 178/2002 of the European Parliament and of the
Council of 28 January 2002 laying down the general principles and requirements of food
law, establishing the European Food Safety Authority and laying down procedures in
matters of food safety.
http://ec.europa.eu/food/food/foodlaw/traceability/index_en.htm. Accessed July 3, 2007.
EU. 2005. Regulation (EC) No 178/2002 of the European Parliament and of the Council
of 28 January 2002 laying down the general principles and requirements of food law,
establishing the European Food Safety Authority and laying down procedures in matters
of food safety.
http://ec.europa.eu/food/food/foodlaw/traceability/index_en.htm. Accessed July 3, 2007.
FAO. 2002. Food and Agriculture Organization. National food control systems assuring
food safety, FAO/WHO Global Forum of Food Safety Regulators, Marrakech, Morocco,
28 - 30 January 2002. GF/CRD FAO-1.
FDA/FSIS/CDC. 2003. Quantitative assessment of relative risk to public health
from foodborne Listeria monocytogenes among selected categories of ready-to-eat foods.
http://www.foodsafety.gov/~dms/lmr2-1.html. Accessed June 29, 2007.
FSA. 2007. Sudan dyes. Food Standards Agency, UK.
http://www.food.gov.uk/safereating/chemsafe/sudani/. Accessed July 5, 2007.
FSIS. 2007. Microbiological results of raw ground beef products analyzed for
Escherichia coli O157:H7. Food Safety and Inspection Service, USDA.
http://www.fsis.usda.gov/Science/Ground_Beef_E.coli_Testing_Results/index.asp.
Accessed June 28, 2007.
Gerner-Smidt P; Hise K; Kincaid J; Hunter S; Rolando S; Hyytia-Trees E; Ribot EM;
Swaminathan B. 2006. PulseNet USA: a five-year update. Foodborne Pathog. Dis. 3(1):
9-19.
Greenwood, M.H. and Hooper, W.L. 1983. Chocolate bars contaminated with
Salmonella napoli. Brit. Med. J. 286: 1394.
Greig, J. D., E. C. D. Todd, C. A. Bartleson, and B. Michaels. 2007. Outbreaks where
food workers have been implicated in the spread of foodborne disease. Part 1.
Description of the problem, methods and agents involved. J. Food Prot., 70: 1752-1761.
24
Halliday, J. 2007. Speakers set out challenges for EFSA's future. FoodNavigator.com
Europe http://www.foodnavigator.com/news/ng.asp?
n=81528&m=1fnen21&c=epfadfzbkiaduyg. Accessed November 21, 2007.
Hargrove, T. 2006. A Russian roulette of food poisoning in American states. November
28, ScrippsNews. http://www.scrippsnews.com/fatalfood. Accessed June 29, 2007.
Healthy People 2010. 2006. Food Safety Midcourse Review.
http://www.healthypeople.gov/data/midcourse/pdf/fa10.pdf. Accessed June 29, 2007.
Hennessy, TW, Hedberg CW, Slutsker L, White KE, Besser-Wiek JM, Moen ME,
Feldman J, Coleman WW, Edmonson LM, MacDonald KL, Osterholm MT. 1996. A
national outbreak of Salmonella enteritidis infections from ice cream. The Investigation
Team. New Engl. J. Med. 334(20):1281–1286.
Henning, K. J. 2004. What is Syndromic Surveillance? MMWR 53 Suppl:7-11.
Johnston, T. 2007a. Irish firm violated France's BSE embargo on British beef: report.
Meatingplace January 23. Meatingplace.com.
Laine, E.S., Scheftel, J.M., Boxrud, D.J., Vought, K.J., Danila, R.N., Elfering, K.M., and
Smith, K.E. 2005. Outbreak of Escherichia coli O157:H7 infections associated with
nonintact blade-tenderized frozen steaks sold by door-to-door vendors. J Food Prot.
68(6):1198–1202.
Mead, P., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M.,
and Tauxe, R. V. 1999. Food-related illness and death in the United States. Emerg.
Infect. Dis. 5: 607-625.
Michino H, Araki K, Minami S, Takaya S, Sakai N, Miyazaki M, Ono A, Yanagawa H.
1999. Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai
City, Japan, associated with consumption of white radish sprouts. Am. J. Epidemiol.
150(8):787–796.
M'ikanatha NM; Rohn DD; Robertson C; Tan CG; Holmes JH; Kunselman AR; Polachek
C; Lautenbach E. 2006. Use of the internet to enhance infectious disease surveillance and
outbreak investigation. Biosecur. Bioterror (3): 293-300.
MMWR. 2005. Progress in improving state and local disease surveillance--United States,
2000-2005. 54(33): 822-825.
MMWR. 2007a. Multistate Outbreak of Salmonella Serotype Tennessee Infections
Associated with Peanut Butter --- United States, 2006—2007. 56(21): 521-524.
http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5621a1.htm. Accessed June 29, 2007.
25
MMWR. 2007b. Preliminary FoodNet data on the incidence of infection with pathogens
transmitted commonly through food --- 10 States, 56(14): 336-339.
Muscatello, D.J., Churches, T., Kaldor, J., Zheng, W., Chiu, C., Correll, P. and Jorm, L.
2005. An automated, broad-based, near real-time public health surveillance system using
presentations to hospital Emergency Departments in New South Wales, Australia. BMC
Public Health 5:141.
Olsen, S.J., MacKinon, L.C., Goulding, J.S., Bean, N.H., and Slutsker, L. 2000.
Surveillance for Foodborne Disease Outbreaks --United States, 1993-1997. MMWR.
March 17, 2000 / 49(SS01): 1-51.
Sinclair, U. 1906. The Jungle. Doubleday, Page & Company, New York.
Smelser, C. 2004. Outbreak of Salmonellosis associated with beef jerky in New Mexico.
2004(3), March 19. New Mexico Epidemiology Report, New Mexico Department of
Health. http://www.health.state.nm.us/pdf/Beef-Jerky-ER-022704.pdf. Accessed July 2,
2007.
Todd, E. C. D. 2001. Surveillance of foodborne disease. In Foodborne Disease
Handbook: Diseases Caused by Bacteria, Hui, Y.H., Pierson, M. D., and Gorham, J. R.
(eds.) 2nd edition. Marcel Dekker, Inc., New York, pp. 515-585.
Todd, E.C.D, C.K. Harris, A.J Knight, and M.R. Worosz. 2007a. Spinach and the media:
how we learn about a major outbreak. Food Protect. Trends. 27(5): 314-321.
Todd, E. C. D., J. D. Greig, C. A. Bartleson, and B. S. Michaels. 2007b. Outbreaks where
food workers have been implicated in the spread of foodborne disease: Part 2: description
of outbreaks by size, severity and settings. J. Food Prot. 70: 1975-1993.
Todd, E. C. D., J. D. Greig, C. A. Bartleson, and B. Michaels, 2007c. Outbreaks where
food workers have been implicated in the spread of foodborne disease. Part 3: Factors
contributing to outbreaks and description of outbreak categories. J. Food Prot., 70: 2199-
2217.
Todd, E. C. D. and Narrod, C. 2006. Agriculture, food safety, and foodborne diseases. In
Understanding the Links between Agriculture and Health. C. Hawkes and M. T. Ruel
(eds.). International Food Policy Research Institute
http://dx.doi.org/10.2499/2020focus13. Accessed July 5, 2007.
USDA. 2007. Interim melamine and analogues safety/risk assessment. May 24, 2007.
http://www.usda.gov/wps/portal/usdahome?
contentidonly=true&contentid=2007/05/0129.xml. Accessed July 3, 2007.
26
Valenciano M; Bergeri I; Jankovic D; Milic N; Parlic M; Coulombier D. 2004.
Strengthening early warning function of surveillance in the Republic of Serbia: lessons
learned after a year of implementation. Euro. Surveill. 9(5): 24-26.
Verdenius, F. 2006. Using traceabilty systems to optimize business performance. In
Improving Traceability in Food Processing and Distribution. I. Smith and A. Furness
(Eds). CRC Press, Woodhead Publishing Ltd, Cambridge, England. pp. 26-51.
Werber, D., Dreesman, J., Feil, F., van Treeck, U., Fell, G., Ethelberg, S., Hauri, A.M.,
Roggentin, P., Prager, R., Fisher, I.S.T., Behnke, S. C., Bartelt, E., Weise, E., Ellis, A.,
Siitonen, A., Andersson, Y., Tschäpe, H., Kramer, M.H., and Ammon, A. 2005.
International outbreak of Salmonella Oranienburg due to German
chocolate. BMC Infect. Dis. 5:7. This article is available from:
http://www.biomedcentral.com/1471-2334/5/7. Accessed June 28, 2007.
WHO. 2004. World Health Organization Global Salm-Surv: A worldwide capacity
building program for the surveillance of Salmonella and other food borne pathogens.
Second FAO/WHO Global Forum of Food Safety Regulators. Bangkok, Thailand, 12-14
October 2004.
http://www.who.int/salmsurv/activities/bulletin_board/en/Attachment_ConferenceRoom
Mess1504.pdf. Accessed July 2, 2007.
WHO. 2006. WHO Global Salm-Surv Progress Report 2000-2005.
http://www.who.int/salmsurv/GSSProgressReport2005_2.pdf. Accessed January 4, 2008.
WHO. 2007. Food safety and foodborne illness. Fact sheet N°237, Reviewed March 2007
World Health Organization http://www.who.int/mediacentre/factsheets/fs237/en/.
Accessed November 20, 2007.
27
A preview of this full-text is provided by CABI.
Content available from CABI Reviews
This content is subject to copyright. Terms and conditions apply.
