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Rev. sci. tech. Off. int. Epiz., 2004, 23 (2), 513-533
Emerging food-borne zoonoses
J. Schlundt (1), H. Toyofuku (2), J. Jansen (2) & S.A. Herbst (3)
(1) Director, Food Safety Department, World Health Organization, 20, Avenue Appia, CH-1211 Geneva 27,
Switzerland
(2) Food Safety Department, World Health Organization, 20, Avenue Appia, CH-1211 Geneva 27, Switzerland
(3) Department of Biochemistry, University of Wisconsin, Madison, Wisconsin, USA
The opinions expressed in this article are those of the authors and do not imply any statement of
World Health Organization policy.
Summary
Diarrhoeal diseases, almost all of which are caused by food-borne or waterborne microbial pathogens, are leading causes of illness and death in less
developed countries, killing an estimated 1.9 million people annually at the global
level. Even in developed countries, it is estimated that up to one third of the
population are affected by microbiological food-borne diseases each year. The
majority of the pathogens causing this significant disease burden are now
considered to be zoonotic. The occurrence of some of these zoonotic pathogens
seems to have increased significantly over recent years.
The factors involved in such increases have not been well studied, but they are
generally agreed to include changes in animal production systems and in the
food production chain. Both types of changes can cause corresponding changes
in patterns of exposure to the pathogens and the susceptibility pattern of the
human population.
This paper will not attempt a more in-depth analysis of such factors. The authors
briefly describe five of the most important emerging food-borne zoonotic
pathogens: Salmonella spp., Campylobacter spp., enterohaemorrhagic
Escherichia coli, Toxoplasma gondii and Cryptosporidium parvum. The paper
does not include a full description of all important emerging food-borne
pathogens but instead provides a description of the present situation, as regards
these globally more important pathogens. In addition, the authors describe each
pathogen according to the new framework of a Food and Agriculture
Organization (FAO)/World Health Organization (WHO) microbiological risk
assessment, which consists of hazard identification and characterisation,
exposure assessment and risk characterisation. Moreover, the authors provide a
brief account of attempts at risk mitigation, as well as suggestions for risk
management for some of these pathogens, based on thorough international
FAO/WHO risk assessments. The authors emphasise the importance of sciencebased programmes for the continued reduction of pathogens at relevant points
of the ‘farm-to-fork’ food production chain, as this is the only sustainable basis
for further reducing risks to human health in the area of preventable food-borne
diseases.
Keywords
Campylobacter – Cryptosporidium – Enterohaemorrhagic Escherichia coli – Food-borne
disease – Microbiological risk assessment – Pathogen – Salmonella – Toxoplasma.
Introduction
There are an enormous number and variety of potential
contamination sources along the food processing chain,
and thus it is unrealistic to imagine that all food can be
kept free from contamination throughout the production
process. However, advances in the 20th Century, such as
pasteurisation,
refrigeration
and
more
recent
improvements in hazard analysis and control along the
production chain, have contributed to improvements in
514
the microbiological safety of most foods. Nevertheless,
food-borne disease remains a significant cause of morbidity
and mortality both in the developed and above all in the
developing world.
A recent national surveillance study in England and Wales
revealed that one in five people develop infectious intestinal
diseases each year, and that Campylobacter and Salmonella
were the most common bacterial pathogens isolated (67). In
the United States of America (USA), it has been estimated
that food-borne diseases may cause up to 76 million
illnesses, 325,000 hospitalisations and 1,800 deaths each
year (44). Extrapolating these data to the rest of the world
would mean that up to one third of the population in
developed countries are affected by microbiological foodborne diseases each year, while the problem is likely to be
even more widespread in developing countries (37). The
poor are the most susceptible to ill health. Food and waterborne diarrhoeal diseases, for example, are the leading causes
of illness and death in less developed countries, killing an
estimated 1.9 million people annually, most of whom are
children (73).
In the estimations from the USA (44), Campylobacter, nontyphoidal
Salmonella
and
enterohaemorrhagic
Escherichia coli (EHEC) account for the vast majority of
bacterial
food-borne
disease
cases
requiring
hospitalisation, whereas Toxoplasma gondii accounts for the
great majority of severe cases of parasitic infections.
Traditionally, food safety efforts have focused on a number
of toxicogenic bacterial pathogens, such as Staphylococcus,
Clostridium and Bacillus. However, it seems that some
important new problems have emerged. This short paper
will briefly describe five of the most important emerging
food-borne pathogens involved in animal production,
as follows:
– Salmonella spp.
– Campylobacter spp.
– EHEC
– T. gondii
– Cryptosporidium spp.
It is not the intention of the authors to give a full
description of all emerging food-borne pathogens but to
try to outline the global situation in regard to some of the
more important pathogens. It should be noted, however,
that the contribution of human caliciviruses
(‘Norwalk-like virus’ and ‘Sapporo-like virus’) to the
infectious intestinal disease burden, has recently been
evaluated in several countries. These caliciviruses are now
estimated to be the cause of 13% to 17% of all the disease
cases in the community that could be attributed to an
infectious agent. Since a significant number of these
infections are also due to food consumption, more work on
food-borne viruses is clearly needed.
Rev. sci. tech. Off. int. Epiz., 23 (2)
Although the authors use the formal headings of
microbiological risk assessment, as defined in the Codex
Alimentarius and applied by the recurrent Joint Food and
Agriculture Organization/World Health Organization
(FAO/WHO) Expert Meetings on Microbiological
Risk Assessment, this paper does not intend to present
either a qualitative or quantitative risk assessment for these
five significant pathogens. The headings have been chosen
to emphasise the importance of this new scientific
discipline, as well as its inherent linkages to several
existing disciplines, including epidemiology, clinical
microbiology, applied microbiology and mathematical
modelling. Moreover, the use of these headings indicates
the potential for this new discipline to allow both better
focused and better monitored disease control measures,
eventually resulting in significant risk reductions.
As defined by WHO and the FAO, risk assessment (the
scientific evaluation of known or potential adverse health
effects) is an integral part of risk analysis, which also
includes risk management (i.e. evaluating, selecting and
implementing different courses of action) and
risk communication (exchanging information among all
interested parties). The four steps of risk assessment are
presented in Figure 1 (74); they are, as follows:
– hazard identification
– exposure assessment
– hazard characterisation
– risk characterisation.
Hazard
identification
Hazard
characterisation
Exposure
assessment
Risk
characterisation
Fig. 1
The four steps of a microbiological risk assessment (74)
Hazard identification involves identifying micro-organisms
as hazards of concern in the relevant food.
Exposure assessment provides an estimate, with an
associated level of uncertainty, of the occurrence and
amount of the pathogen in a specified portion of food at
the time of consumption.
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Rev. sci. tech. Off. int. Epiz., 23 (2)
Hazard characterisation provides a description of the
adverse effects that may result from ingestion of a microorganism and presents a dose-response relationship.
Risk characterisation is the integration of the three
previous steps to obtain a risk estimate, i.e. an estimate of
the likelihood and severity of the adverse effects which will
occur in a given population, with an associated level of
uncertainty.
Thermophilic
Campylobacter species
Introduction
It was already established in the 1970s that thermophilic
Campylobacter was a common cause of bacterial
gastroenteritis in humans (59). However, Campylobacter is
now the leading cause of zoonotic enteric infections in
most developed and developing countries (70). Most
human Campylobacter infections are classified as sporadic
single cases or as part of small family-related outbreaks.
Identified outbreaks are not common.
The reported incidence of Campylobacter infections has
markedly increased in many developed countries within
the last twenty years (Fig. 2).
Hazard identification and characterisation
Food-borne campylobacteriosis is associated mostly with
C. jejuni (which is frequently isolated from chickens) and, to
a lesser degree, with C. coli (often found in pigs). The
principal reservoir of pathogenic Campylobacter spp. is the
alimentary tract of wild and domesticated mammals and
birds. It is evident that Campylobacter is commonly found in
broilers, broiler breeder flocks, cattle, pigs, sheep, wild
animals and birds, as well as in dogs (5). In water and other
environments with sub-optimal growth conditions,
Campylobacter may convert into a ‘viable but non-culturable’
state. The importance of this ‘state’ in the transmission of
Campylobacter to animals and people is not clear.
The pathogenesis of Campylobacter is poorly understood.
Several determinants of virulence have been described, but
their relative roles and importance in the development of
diarrhoea are not clear. Enteropathogenic Campylobacter
can cause an acute enterocolitis, which is not easily
distinguished from illness caused by other enteric
pathogens. The incubation period may vary from one to
eleven days, but typically lasts between one and three days.
The main symptoms are as follows:
– malaise
– fever
– severe abdominal pain
– diarrhoea.
140
Incidence (cases/100,000)
120
100
80
60
40
20
10
0
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
Year
England & Wales
Denmark
Switzerland
Israel
Iceland
Finland
Sweden
Norway
Slovakia
Scotland
Fig. 2
The reported incidence of campylobacteriosis in ten European countries between 1985 and 1998 (63)
516
Campylobacter infections may be followed by rare but
severe non-gastro-intestinal sequelae, e.g. reactive arthritis,
Guillain-Barré syndrome and Miller Fisher syndrome. In
general, very few deaths are related to Campylobacter
infections and these deaths usually occur among infants,
the elderly and people whose immune systems are
suppressed (2).
In general, most human Campylobacter infections are selflimiting and do not need antimicrobial therapy. However,
in severe cases, medication may be necessary. In the
beginning of the 1990s, fluoroquinolone-resistant C. jejuni
and C. coli emerged in human populations in Europe, as
reported in the United Kingdom (UK), Austria, Finland
and the Netherlands. This resistance has been linked to the
approval of enrofloxacin for the treatment of diseases of
broiler chickens. Investigations have shown that
fluoroquinolone-sensitive C. jejuni strains were able to
convert to resistant forms when fluoroquinolone was
added to broiler chicken feed (35). Fluoroquinoloneresistant Campylobacter from chicken and other poultry is
an emerging public health problem. Although lower levels
of resistance are reported in many countries, the
percentage of fluoroquinolone-resistant strains of
Campylobacter has been shown to be high in Taiwan
(57%), Thailand (84%) and Spain (88%) (40). It is
important to realise that the countries reporting such
prevalences are not necessarily the countries with the
highest real prevalence, since many countries do not have
any reporting mechanisms.
In developed countries, all age groups may become
infected with Campylobacter. However, in most countries,
the reporting rate of campylobacteriosis is higher in young
children (from birth to four years old) and young adults.
The high incidence rate in children may be a result of
higher susceptibility, more frequent exposure (to
companion animals, for example), or a higher notification
rate in this age group as compared to adults, reflecting the
fact that parents are more likely to seek medical care for
their children. In developing countries, illness is more
common among infants and children and it is suggested
that young adults and adults have acquired immunity as a
result of repeated exposures (70).
Exposure assessment
As Campylobacter is common in the faeces of warmblooded animals, inevitably the meat will be contaminated
during slaughter. Thermophilic Campylobacters have an
optimum growth temperature of 42°C and no growth
below 32°C. Thus, it is reasonable to assume that
Campylobacter spp. do not multiply during slaughtering,
after processing or during transport and storage. In regard
to cattle and pigs, Campylobacter concentrations have been
shown to decline during the slaughtering processes.
Broiler-chicken processing can reduce levels of
Rev. sci. tech. Off. int. Epiz., 23 (2)
Campylobacter on the skin by up to 100-fold (43). In
various food items, Campylobacter survival has been
recorded after several weeks of storage at 4°C, and after
several months in frozen poultry.
In many countries, poultry meat in particular has been
found to be contaminated with Campylobacter (up to
75% of all retail chicken samples tested positive). Lower
prevalences of Campylobacter have been found in beef,
pork, other meat products, raw milk, milk products and
fish and fish products. More rarely, Campylobacter has also
been found in vegetables.
Outbreaks and sporadic cases seem to have different
epidemiological characteristics. For example, sporadic
cases seem to peak in summer, whereas outbreaks (based
on data from 57 outbreaks in the USA) seem to culminate
in May and October (60).
The following major risk factors have usually been
associated with outbreaks of campylobacteriosis:
– consumption of poultry
– drinking unpasteurised milk
– contact with untreated surface water
– contaminated public and private water supplies (50).
Cross-contamination of Campylobacter from raw chicken to
prepared food has also been identified as a risk factor. A
link was observed between infection and not washing the
kitchen cutting board with soap (31).
The possible risk factors related to sporadic cases of human
campylobacteriosis have been investigated in several casecontrol studies (38, 50). Most studies have identified
handling raw poultry and eating poultry products as
important risk factors, which account for a variable
percentage of cases. Other food-related risk factors that
have repeatedly been identified include consumption of
other meat types, consumption of undercooked or
barbecued meat, etc. Travel, contact with animals and
recreational activities in natural surroundings are also
known risk factors (46, 50). Several investigations have
pointed out that having contact with companion animals,
particularly young animals such as kittens and puppies,
significantly increases the risk of Campylobacter infection
(9, 50).
Water is an important part of the ecology of Campylobacter.
Campylobacter has, in some regions, been isolated from
surface water, rivers and lakes at prevalences of up to about
50% during cold winter months (12). The higher winter
prevalence is explained by a higher survival rate at low
temperatures and in shorter periods of daylight (10).
Recent research in Finland indicates that swimming in
natural sources of water is an independently associated risk
for sporadic Campylobacter infection (58).
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Rev. sci. tech. Off. int. Epiz., 23 (2)
Poultry and other foods are thought to be the most likely
potential sources of infection in many developed countries.
However, in some developing countries, water-borne
transmission, direct contact with animals and
environmental sources are thought to be the major routes
of human infection (70). In other countries, poultry living
in the household or within close proximity of the
household serve as sources for the organism. For instance,
in Peru and Cameroon, chickens in the household have
been shown to lead to household members being exposed
to Campylobacter infection (39).
Risk characterisation
The incidence rates of Campylobacter infections vary
widely, which may partly be explained by differences in
surveillance systems. The true rate of infection is higher
than the number of reported cases (from 7.6 up to 100
times as high) (67, 44).
The burden of human Campylobacter infections in
developing countries is generally not known. It is likely
that the rate of campylobacteriosis is high, especially
among children below two years of age (11).
Campylobacteriosis
significantly
contributes
to
malnutrition in infants, as the illness is particularly acute
during the weaning period (70).
The FAO/WHO assessment of Campylobacter in broiler
chickens presents a model that includes all stages of the
chicken production chain, and can be used to generate
baseline estimates of the risk of Campylobacter infection on
a per-serving basis (25). The model evaluates the impact of
various mitigation measures, such as chlorination in chill
tanks and freezing, on the level of risk. Each stage of the
supply chain is described as a separate module. Since each
of these modules can be used separately or in combination,
the overall model is potentially adaptable to the specific
situation in each country. The baseline model is defined as
a system with an overall flock Campylobacter prevalence of
80%, in which chickens are water chilled without free
chlorine, and sold fresh (refrigerated but not frozen).
To characterise the risks of a specific system fully, the
features of that system must be accurately captured and the
data particular to that situation must be applied. It is
possible to use alternative data but, in that case, such data
must be carefully screened, to ensure that they are
appropriate. Every system is likely to be different to some
degree, just as every country is likely to have its own
particular systems.
Constructing a model of a system (in this case, a chicken
production/processing system) and examining it under
various scenarios provides valuable insights into how the
‘real-life’ system would behave under those circumstances.
The model can be used to reflect the particular realities that
the scientists want to explore. In the FAO/WHO
assessment, several scenarios were constructed. The results
can be briefly summarised, as follows (25).
a) If the level of Campylobacter contamination is
reasonably high, then reducing the frequency with which
chickens are contaminated provides a greater return on
investment than reducing the level of contamination.
However, if the level of contamination is reasonably low,
reducing the frequency of contamination is likely to be less
effective than reducing the level of contamination further.
b) Reducing the ‘between-flock’ prevalence at the farm has
an effect on risk reduction which is slightly greater than a
one-to-one relationship. (In a one-to-one relationship, a
percentage change in herd prevalence reduces the expected
human risk by a similar percentage.) Thus, reducing the
‘between-flock’ prevalence by 50% is estimated to reduce
the risk by slightly less than 50%. Reducing the withinflock prevalence, but maintaining the overall betweenflock prevalence, produces a much lower reduction in risk.
This is primarily due to the fact that the birds from these
flocks are being processed in an environment in which they
are surrounded by infected birds.
c) Reducing surface contamination after evisceration is
estimated to have quite a significant effect. A
90% reduction in the surface contamination level after
evisceration translates into a 63% reduction in the mean
risk overall.
d) Since freezing is known to lower the level of
Campylobacter contamination, it is estimated that frozen
chickens have a lower risk than those that are sold and
stored refrigerated. The difference is best illustrated
through a scenario which demonstrates that an equivalent
level of risk can be maintained for a more heavily
contaminated product if that product is frozen. For
instance, the mean risk for refrigerated chicken at a mean
contamination level of 4.5 log colony-forming units (CFU)
per gram is approximately the same as for frozen chicken
at a mean contamination level of approximately 5.25 log
CFU per gram.
Risk management
Campylobacter ecology at the poultry herd level is still not
clearly understood. There are very few examples of
implementing traditional risk management measures in
poultry production to lower the risk of campylobacteriosis
in the human population.
All elements of risk assessment, as presented above,
contribute to providing risk managers with accurate
information on the magnitude of the risk in question, as
well as on potential mitigation strategies and their expected
effectiveness.
518
Although a new risk management protocol is still being
developed by the FAO/WHO Codex Alimentarius
Commission, several countries have already attempted to
reduce the burden of campylobacteriosis through a
structured approach, which includes the scientific insights
gained from risk assessments (7). The control measures
applied include the following examples:
– in Iceland, the general application of freezing after
slaughter
– in Denmark, testing flocks one week before slaughter,
and only allowing the distribution of slaughtered birds
from a flock as fresh meat after the flock has tested negative
for the presence of Campylobacter
– in several countries, separating flocks that test positive
for the presence of Campylobacter from flocks that test
negative, enabling the distribution of ‘Campylobacter-free’
poultry meat
– in the USA, reducing Campylobacter contamination of
consumer products through the use of water chlorination
during poultry slaughtering
– in Sweden, lowering the herd prevalence of
Campylobacter in poultry production.
In discussing risk management efforts for most food-borne
pathogens, the role played by those who finally prepare the
food, whether in the home or in professional kitchens,
should not be underestimated. For Campylobacter, as for
the other pathogens described in this paper, educating the
public about a few, relatively simple key precautions when
preparing or preserving food would probably have a
significant effect on lowering the risk of disease.
As a result, WHO has developed a simple educational
campaign based around the ‘Five keys to safer food’ poster
(71), as well as training material aimed at different
audiences, such as children, ordinary consumers, street
food vendors, etc. In brief, the ‘Five keys to safer food’ are
as follows:
– keep clean
– separate raw and cooked
– cook food thoroughly
– keep food at safe temperatures
– use safe water and raw materials.
Several national food safety authorities are promoting
similar messages but a more coherent global effort is
needed to encompass more countries and, in particular,
developing countries.
Cryptosporidium parvum
Introduction
Cryptosporidium species are intestinal protozoan parasites
which are excreted in animal faeces as stable oocysts.
Rev. sci. tech. Off. int. Epiz., 23 (2)
Cryptosporidium has been detected in the faeces of a wide
range of ruminant and non-ruminant animals, including
farmed animals, wild animals, domestic companion
animals and birds. It is known that young animals are
frequent (faecal) carriers of oocysts of C. parvum. Thus,
C. parvum has been identified as a potential hazard for food
products or water reservoirs, which are likely to be
contaminated with animal faeces or animal production
run-off.
This parasite appears to be well adapted to survive and
persist in faeces for extended periods, ranging from several
weeks to many months. Because of this persistence, faeces
are important potential vehicles of transmission within
herds, farms, the water chain, the fresh food chain and the
wider environment. It was only when the United States
Centers for Disease Control and Prevention (CDC)
reported Cryptosporidium as the causative agent of severe
protracted diarrhoea in acquired immune deficiency
syndrome (AIDS) patients that this parasite was recognised
as an important human pathogen (15). In the 1990s, it was
recognised as one of the leading known causes of waterborne disease outbreaks and an important cause of
diarrhoea outbreaks in day-care centres.
Hazard identification and characterisation
Since the first human cases were documented in 1977,
C. parvum can be termed an emerging pathogen.
Outbreaks have typically been associated with the
consumption of contaminated water or food (23, 45).
Although there are few reports of food-related outbreaks,
since such outbreaks seem difficult to document and are
greatly under-reported, water-borne outbreaks have been
documented often. Reports of water-borne outbreaks show
a combination of causes, including contaminated source
water, high turbidity and failures at the treatment plant
(23). Other vehicles for transmission also exist, including
recreational waters.
To date, the genus Cryptosporidium consists of at least ten
recognised species. However, human infection is
predominantly caused by C. parvum (23). The incubation
period varies significantly but is usually around seven days
(72). The disease is usually self-limiting, and symptoms
normally last between three and twelve days. After
infection, abdominal pain, nausea, fever and, in particular,
diarrhoea can occur. Both the probability of infection and
the probability of illness depend on the viability of the
oocysts and the health of the consumer. Immunosuppressed individuals are at greater risk. For these people,
especially the elderly and AIDS patients, diarrhoea can be
severe, persistent and may even be life-threatening (41).
Current and Garcia (20) reviewed more than 100 studies
on the prevalence of Cryptosporidium in people from over
40 countries. They noted that the prevalence rates in the
more industrialised countries of North America and
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Rev. sci. tech. Off. int. Epiz., 23 (2)
Europe were between 1% and 3%, whereas, in
underdeveloped countries, rates ranged from 5% in Asia to
10% in Africa, with some increases during the warmer
and/or wetter months.
Models for dose-response relations have been described for
C. parvum (29, 61). These models are based on data from
human feeding trials. The probability of illness is
determined by the probability of illness caused by a single
oocyst (termed the R-value) multiplied by a mathematical
function of the number of oocysts ingested. The function
which best fitted the data was an exponential function,
thereby leading to an exponential dose-response model.
The R-value was estimated to be 0.0042 by Teunis et al.
(61). Since infectivity is likely to increase among the AIDS
population, Perz et al. (55) used a three-fold higher
infectivity for people with AIDS.
This dose-response model, however, contains a great deal
of uncertainty. Hoornstra and Hartog (32) calculated
the mean probability of illness at different doses using the
exponential dose-response model, resulting in a mean
probability of infection when ingesting 100 viable oocysts
of 35%, and a mean probability of infection when ingesting
10 viable oocysts of 5%. The predictions for a few
oocysts are uncertain, but the extrapolation of the model
will result in a certain probability of becoming ill from a
single oocyst, because of the choice of a non-threshold
model. The mean probability of infection when the dose is
1 oocyst is 0.4%. The mean probability of illness
(cryptosporidiosis) after such infection is 61%, resulting in
a probability of illness of 0.25%.
Exposure assessment
The organism C. parvum can be transmitted to humans
through a number of routes, as follows:
– person-to-person infection
– human-to-water-to-human infection
– animal-to-human infection
– water-borne infection (from potable, surface and
recreational water)
– food-borne infection.
In fact, C. parvum cannot replicate in food, but oocysts can
potentially survive in contaminated foods and infect
people, either directly, as a result of eating raw or
undercooked food, or indirectly, as a result of
cross-contamination. Mead et al. (44) assumed that 10% of
cases in the USA were attributable to food-borne
transmission, with the rest caused by the consumption of
contaminated water or person-to-person transmission.
Foods of animal origin, including raw milk and/or dairy
products, raw meats and fresh fruit and vegetables which
have been produced in a contaminated environment, are
most likely to pose a risk to humans.
Outbreaks of cryptosporidiosis due to C. parvum have
recently been linked to dairy products (pasteurised bovine
milk and raw goat milk), apple cider and meat products,
including chicken salad, frozen tripe and raw sausages
(23, 45). It is usually difficult to identify the source of
infection due to the relatively long incubation period (2 to
11 days). In addition, the lack of suitable methods for the
routine detection of this parasite in foods has also
hampered epidemiological investigations (54).
Reduction in viability is an important factor. To evaluate
the risk to the consumer, it is also necessary to calculate the
numbers of Cryptosporidium at the point of consumption
and to know the quantity of food consumed.
Risk characterisation
Even though Hoornstra and Hartog (32) reported that the
mean probability of illness from the consumption of tap
water was 1.5 x 10-5 per year in the Netherlands, and Perz
et al. (55) estimated that the median risk of infection from
tap water for adults without AIDS was 9 infections per
10,000 persons per year in the USA, there are no
quantitative risk assessments of Cryptosporidium in food in
the literature.
The annual incidence rate was 21.2 cases per 100,000
persons in New Zealand in 2000 (51). Mead et al. (44)
estimated
approximately
300,000
cases
of
cryptosporidiosis per year in the USA (approximately 100
cases per 100,000 persons). Specific groups at risk of
infection included the following:
a) children under five years of age
b) malnourished people
c) a range of immuno-compromised individuals,including:
– AIDS patients
– transplant recipients
– patients receiving chemotherapy for cancer
– institutionalised patients
– patients with
diseases (23).
immuno
suppressive
infectious
Various surveys have indicated that the oocyst prevalence
in human faeces ranges from 1% to 2% in Europe, 0.6% to
4.3% in North America and 10% to 20% in the developing
countries. However, serological evidence of past infections
has shown positive rates of 25% to 35% in industrial
countries and up to 65% in developing countries (1).
520
Risk management
To control the transmission of C. parvum through the food
chain, a ‘farm-to-fork’ approach must be taken, with efforts
focused at various points along the chain. On-farm
controls should include managing livestock to reduce the
transmission of infection between animals and the
contamination of the farm environment. Of equal
importance are the correct storage and/or treatment of
animal wastes to limit the transmission of the parasite to
the farm environment, where, as reported above, it may
survive
for
considerable
periods.
Since
C. parvum has been involved in major outbreaks, following
the contamination of water reservoirs with animal
production run-off, on-farm efforts to prevent transmission
through animal wastes are seen as crucial. Active treatment
processes of animal wastes that are currently used include
composting, heat-drying and anaerobic digestion.
Millar et al. (45) indicated that the parasite is introduced to
foodstuffs through the following:
a) contaminated raw ingredients, e.g. unwashed lettuce
destined for ‘ready-to-eat’ salads
b) the addition of contaminated water as an important
ingredient of the foodstuff during processing, e.g. in soft
drinks production
c) contamination while cleaning equipment with nonpotable water or contaminated potable water during
processing
d) pest infestations, e.g. due to cockroaches, house flies,
mice and rats
e) introduction of the parasite into processed foodstuffs by
infected food handlers.
The associated risk from each of these potential entry
routes of oocysts into the foodstuff should be controlled
through a ‘good hygienic practice’ and ‘hazard analysis
critical control point’ system approach.
During food processing, common disease control measures
may be successful in reducing or eliminating the parasite.
These measures include the following:
– low pH
Rev. sci. tech. Off. int. Epiz., 23 (2)
raw foods and good hygiene practices in the home, as in
the ‘Five keys to safer food’ poster (71), to avoid the risk
of cross-contamination.
Enterohaemorrhagic
Escherichia coli
Introduction
Escherichia coli is a common inhabitant of the gut of
humans and warm-blooded animals. Most strains of E. coli
are harmless. Some strains, however, such as EHEC, can
cause severe food-borne disease.
The significance of EHEC as a public health problem was
first recognised in 1982, following an outbreak in the USA.
The term EHEC was originally defined as those serotypes
that cause a clinical illness similar to that caused by
E. coli O157:H7 and contain similar virulence
determinants, including a virulence plasmid that encodes
enterohaemolysin (normally referred to as verocytotoxin
[VT] – hence the term VTEC for positive strains). Thus,
EHEC is now used as a term for VTEC strains that cause
haemorrhagic colitis in humans.
In many countries, including the UK and the
USA, E. coli O157:H7 is currently the most predominant
food-borne EHEC. However, it is not the only
EHEC strain associated with food-borne disease. A number
of other O-serotypes of E. coli, such as O26, O103, O111,
O118 and O145, cause significant morbidity in
many countries (8). Although the overall incidence of
disease
caused
by
EHEC
is
low,
the
life-threatening complications of infection in young children
and the elderly are cause for serious concern.
New research in this area seems to indicate that EHEC is
fairly prevalent in the bovine intestine, but uncertainties
about the isolation, typing and virulence characterisation of
this subgroup of the intestinally ubiquitous E. coli complicate
the picture (69).
Hazard identification and characterisation
– heating at 55°C for 30 seconds, 60°C for 15 seconds or
70°C for 5 seconds.
Most of the available information on EHEC is related to
serotype O157:H7, which is easily differentiated
biochemically from other E. coli strains because it ferments
sorbitol slowly.
It should be noted that a combination of filtration and
disinfection is required to control C. parvum in water, since
chlorination alone has not been successful in eliminating
water-borne C. parvum oocysts (45). At the domestic level,
as with all food-borne pathogens, the risk of
cryptosporidiosis can be reduced by adequate cooking of
Ordinary E. coli strains colonise the gut of an infant
within a few days of birth, typically from the mother by the
faecal-oral route or from the environment. While results
from the oral challenge of volunteers suggest that
levels of 105 to 1010 of other types of pathogenic E. coli are
necessary for infection, epidemiological evidence
– freezing
521
Rev. sci. tech. Off. int. Epiz., 23 (2)
suggests that the risk of disease from EHEC can be high
even at very low doses (<1,000 bacteria) (66). This would
traditionally be expressed as ‘a very low infectious dose’,
but this statement can also be misinterpreted as meaning
that any person given a dose of 1,000 EHEC
bacteria will become sick. Since this is not the case,
scientists prefer to use a measure called the
‘dose-response’, meaning that a certain percentage of a
particular group of people who receive a pre-determined
amount of EHEC will get sick. This percentage is normally
referred to as the ‘attack rate’. The Food Safety
and Inspection Service in the USA recently carried out a
risk assessment of E. coli O157:H7 by comparing the
dose-response of EHEC with that of Shigella dysenteriae, for
which better data exist. Using this model, the
50% attack rate for both bacteria is reached at
approximately 750 micro-organisms. However, data from
EHEC
outbreaks demonstrate that doses below
50 micro-organisms can result in significant attack rates,
especially among the young and the old (6).
contamination during the slaughter process, an average
total of 43% of animals coming out of the slaughter line are
contaminated with the pathogen (6).
Humans are infected with EHEC primarily through the
consumption of contaminated foods, such as raw or
undercooked ground meat products and raw milk. Faecal
contamination of water and other foods, as well as crosscontamination during food preparation (originating from
beef and other meat products, contaminated surfaces and
kitchen utensils), can also cause infection. Examples of
foods implicated in outbreaks of E. coli O157:H7 include
the following:
– undercooked hamburgers
– dried, cured salami
– unpasteurised fresh-pressed apple cider
– yogurt
– cheese
– milk.
As stated above, EHEC produces toxins. These are known as
verotoxins or Shiga-like toxins because of their similarity to
the toxins produced by Shigella dysenteriae. The
bacterium grows in a temperature range from approximately
7°C to 50°C, with an optimum temperature of 37°C.
Some EHEC can grow in acidic foods, down to a
pH of 4.4, as well as in foods with a minimum
water activity of 0.95. The bacterium is destroyed by
thorough cooking, until all parts of the food reach a
temperature of 70°C.
Symptoms of the disease caused by EHEC include
abdominal cramps and diarrhoea that may, in some cases,
progress to bloody diarrhoea (haemorrhagic colitis). Fever
and vomiting may also occur. The incubation period can
range from 3 to 8 days, with a median of between 3 and
4 days. Most patients recover within 10 days. However, in
a small proportion of patients (particularly young children
and the elderly), the infection may lead to a
life-threatening disease: haemolytic uraemic syndrome
(HUS). This syndrome is characterised by acute renal
failure, haemolytic anaemia and thrombocytopenia.
Exposure assessment
The reservoir for EHEC appears to be principally the
gastro-intestinal systems of cattle and other ruminants.
In individual bovines, investigations seem to indicate a
relatively low animal prevalence of EHEC (1% to 2%) (26).
However, there seems to be a relatively high, but variable,
level of bovine herd prevalence, ranging from 10% in some
countries to nearly 100% in feedlot herds in the USA (6).
However, new data from the USA seem to show that
28% of the animals presented for slaughter could be
infected with E. coli O157:H7, and due to additional
An increasing number of outbreaks are associated with the
consumption of fruit and vegetables (such as sprouts,
lettuce, coleslaw and salad). Since several EHEC outbreaks
have been caused by contaminated sprouts, it was agreed
by the Codex Alimentarius Commission to include sprouts
in the EHEC risk profile study (18).
Sprout contamination is typically due to contact with faeces
from domestic or wild animals at some stage of the
cultivation or handling, in particular the practice of using
animal slurry as fertiliser on fields after germination. The
largest O157 outbreak involved approximately
9,000 Japanese schoolchildren and was caused by
contaminated radish sprouts (69). In general, EHEC has
been isolated in the environment from soil and bodies of
water, especially after the application of animal slurry, and
found to survive for months in these environments (52).
Water-borne transmission has also been reported, both from
contaminated drinking water and from recreational waters.
Person-to-person contact is an important mode of
transmission, and occurs through the oral-faecal route
(69). An asymptomatic carrier state has been reported,
where individuals show no clinical signs of disease but are
capable of infecting others. The period during which
EHEC is excreted is about one week or less in adults, but
can be longer in children. Visiting farms and other venues
where the general public might come into direct contact
with farm animals has also been identified as an important
risk factor for EHEC infection.
Risk characterisation
It is estimated that up to 10% of patients with EHEC
infection may develop HUS, which has a case-fatality rate
522
ranging from 2% to 7% (69). This syndrome is the most
common cause of acute renal failure in young children. It
can cause neurological complications (such as seizure,
stroke and coma) in 25% of HUS patients and chronic
renal sequelae, usually mild, in around 50% of survivors.
The incidence of EHEC infections varies by age group, with
the highest incidence of reported cases occurring in
children aged under 15 years. Data from developed
countries demonstrate that, whereas the general incidence
often varies between 0.1 and 2 cases per 100,000, in
certain regions and time periods this incidence can
increase significantly (69). Data from the USA suggest that
more than two thirds of EHEC cases are the result of
exposure to the pathogen through food (69). The USA data
also suggest that EHEC infections are likely to be
significantly under-reported, since the incidence arrived at
through these estimations is more like 30 cases per
100,000 (44).
The percentage of EHEC infections which progress to HUS
varies between sporadic cases (3% to 7%) and those
associated with outbreaks (20% or more). In
epidemiological terms, there is generally a background of
sporadic cases, with occasional outbreaks. Some of these
outbreaks have involved a high number of cases, such as
the Japanese outbreak cited above. Data on the situation in
developing countries are limited, as surveillance for this
pathogen is not routinely conducted.
Risk management
Preventing infection requires disease control measures at all
stages of the food chain, from agricultural production on
the farm to the processing, manufacturing and preparation
of foods in both commercial establishments and the
domestic environment. The available data are not sufficient
to recommend implementing specific disease control
measures on the farm to reduce the incidence of EHEC in
cattle. Nevertheless, research in this area should be
encouraged as disease control measures at the farm level
are, in most cases, the most cost-effective in the long term.
Risk assessments conducted at the national level have
predicted that the number of cases of disease might be
reduced by various mitigation strategies for beef production.
One such strategy is the thorough screening of animals
before slaughter to minimise the introduction of large
numbers of pathogens into the slaughtering environment
(6). Good hygienic slaughtering practices reduce the
contamination of carcasses by faeces, but do not guarantee
the absence of EHEC from products. It is essential that
abattoir workers and those involved in the production of raw
meat are educated about the hygienic handling of food, to
keep microbiological contamination to a minimum.
Similarly, preventing the contamination of raw milk on farms
Rev. sci. tech. Off. int. Epiz., 23 (2)
which test positive for the presence of EHEC is virtually
impossible, but farm workers should be educated in the
principles of good hygienic practice to keep contamination
to a minimum. On ‘show-case’ and ‘petting’ farms, direct
contact between the animals and the general public should
be guided by strict hygiene rules.
Some countries (e.g. the USA) follow the policy that raw
ground beef is considered adulterated if it is found to contain
E. coli O157:H7. This has led to major recalls of very
significant amounts of beef, typically of ground beef, and has
most likely heightened producer awareness of the problem.
Preventive measures for E. coli O157:H7 infections are
similar to those recommended for other food-borne diseases.
However, some of these measures may need to be reinforced
for EHEC, particularly in view of its importance to
vulnerable groups, such as children and the elderly. Food
handlers and the general public should follow good hygienic
practices, such as those described in the WHO ‘Five keys to
safer food’ poster (71). In particular, the recommendation to
‘cook food thoroughly’ is especially relevant for minced
meat. In cuts of meat, the centre of the meat piece is
normally virtually sterile, whereas bacterial contamination
could be high on the surface. In minced meat, e.g. burgers,
the meat is generally contaminated throughout. Therefore an
item of minced meat should always be cooked to reach
70°C throughout the entire item.
Although, in general, an effective method of eliminating
EHEC from food is to introduce a bactericidal treatment,
such as heating (e.g. cooking or pasteurisation) or
irradiation, a number of important foods are not easily
treated in this way. One very important example is
vegetable sprouts, which are produced for consumption
without heat treatment. Reports of food-borne outbreaks
of EHEC associated with raw sprouts have indicated that
the pathogens found on the sprouts most likely originate
from the seeds, which can be contaminated by liquid
animal manure (slurry). During the germination stage, the
low levels of pathogens present on the seeds may quickly
reach levels high enough to cause disease. Therefore,
specific care is needed, both in the agricultural practices
used to produce seeds for sprouting and in sprout
production practices.
Since a number of EHEC infections have been caused by
contact with recreational water, it is also important to
protect such bodies of water from animal wastes. This also
applies to sources of drinking water.
Salmonella species
Introduction
Salmonellosis is one of the most frequently reported foodborne diseases worldwide. In Europe, Salmonella trends
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Rev. sci. tech. Off. int. Epiz., 23 (2)
have been well-documented over the past 20 years, but in
other parts of the world it is rare to find comparable data
for such a large group of countries for periods as long as
this. According to the WHO surveillance programme for
the control of food-borne diseases in Europe (in which fifty
countries currently participate), incidences of
salmonellosis in Europe have shown a general increase
over the past twenty years (62).
Another example of Salmonella spreading through the
animal population, followed by a corresponding
occurrence of human cases, is demonstrated by the multiresistant Salmonella serovar Typhimurium Definitive
Type (DT) 104. From the beginning of the 1990s,
S. Typhimurium has spread rapidly through many
European countries and North America (and probably
elsewhere), mainly in cattle production systems but also,
later, in pigs (16). An interesting comparison of the relative
increases in DT104 isolates from the bovine and human
populations in the north-west of the USA is presented in
Figure 4 (21).
Since 1985, there has been a significant increase in the
incidence of salmonellosis in many countries. This increase
reached a peak in 1992; even earlier in some countries
(Fig. 3). Similar salmonellosis disease patterns seem to
have evolved in most other regions of the world.
Although many different foods have been implicated in
salmonellosis outbreaks, most cases are usually caused by
the consumption of poultry and eggs. Reflecting this fact,
the FAO and WHO have undertaken a risk assessment of
Salmonella in eggs and broiler chickens, to aid in managing
the risks associated with these products (24). Many
international experts participated in this project, which
will be further referred to below.
In retrospect, this pattern could be regarded as a global
epidemic caused by Salmonella enteritidis, which originated
primarily in the reservoir of infection building up in
intensive poultry production systems. Originally,
S. enteritidis appeared simultaneously around the world in
the 1980s (56). During the 1990s, it was most probably
spreading into the poultry production systems of
developing countries (42).
In several countries, the incidence of salmonellosis has
now decreased due to the implementation of control
measures, including greater public awareness of the risk. In
other countries, the incidence of salmonellosis continues
to increase.
Hazard identification and characterisation
Over 2,000 serotypes of Salmonella have been identified.
The most prevalent are S. enteritidis, S. Typhimurium and
S. Heidelberg.
250
Incidence (cases /100,000)
200
150
100
50
0
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
Year
Estonia
Lithuania
Latvia
Austria
Russian Federation
Switzerland
Cyprus
United Kingdom
Germany
Fig. 3
The reported incidence of salmonellosis in nine European countries between 1985 and 1998 (63)
1998
Rev. sci. tech. Off. int. Epiz., 23 (2)
50
Exposure assessment
40
Foods of animal origin, especially poultry, poultry
products and raw eggs, are often implicated in sporadic
cases and outbreaks of human salmonellosis (13, 34). In
addition, recent years have seen an increase in
salmonellosis associated with contaminated fruits and
vegetables. This contamination is typically due to contact
with faeces from domestic or wild animals at some stage
during cultivation or handling, in particular, the practice of
using animal slurry as fertiliser on the fields after
germination. In general, Salmonella spp. have been isolated
from soil and plants, especially after the application of
animal slurry, and found to be able to survive for months
(depending on the initial level of contamination) in these
environments (49).
30
20
10
0
1982-1985
1986-1990
1991-1994
1995-1996
Year
cattle
humans
Fig. 4
A comparison of the relative increases in isolates of
Salmonella Typhimurium Definitive Type 104, by percentage, in
cattle and human populations in the north-west United States of
America, between 1982 and 1996 (21)
Salmonellosis is characterised by the following symptoms:
– diarrhoea
– fever
– abdominal pain or cramps
– vomiting
– headache
– nausea.
The incubation period ranges from 8 to 72 hours.
Symptoms can last up to a week. Salmonella infections vary
from mild to severe, and are occasionally fatal. Fatalities are
more often seen in susceptible populations, i.e. infants, the
elderly and the immuno-compromised. A small proportion
of infected people may develop Reiter’s syndrome, an
arthritic disease characterised by joint pain, eye irritation
and painful urination.
The appearance of Salmonella strains that are resistant to
antimicrobials is added cause for concern. In addition to
the spread of S. Typhimurium DT104, mentioned above, a
more recent spread of S. Newport strains, which
demonstrate antimicrobial resistance against some of the
new ‘last-line’ antimicrobials (i.e. antimicrobials of last
resort), is worrying. The general threat caused by the nonhuman use of antimicrobials, resulting in resistant zoonotic
pathogens, has led to recent joint activities by the FAO, the
World Organisation for Animal Health and the WHO (75).
The FAO/WHO risk assessment developed a new doseresponse model based mainly on data from Salmonella
outbreaks. This model is considered to be the most
appropriate, internationally recognised model for
predicting illness after the ingestion of a dose of Salmonella.
It was based on observed (outbreak) data, with inherent
uncertainties. These outbreak data are from a limited
number of developed countries and may not apply to other
regions (24). The dose-response model and the
uncertainties contained in it, as well as the outbreak data
used, are presented in Figure 5.
The foodstuffs implicated in outbreaks from Salmonella
spp. in the USA between 1993 and 1997 included, as
follows (18):
– eggs (17 outbreaks)
– beef (13 outbreaks)
– ice cream (10 outbreaks)
– chicken (5 outbreaks)
– pork (16 outbreaks).
Using combined typing to link the strains that cause
disease with those occurring in different foods, the
estimated mean number of sources out of 1,713 cases of
human salmonellosis in Denmark in 2003 were, as follows:
– 271 cases from table eggs
– 230 cases from imported poultry
1.0
0.9
0.8
Probability of illness
Percentage increase
524
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
0
1
2
3
4
5
6
7
8
9
10
Log dose
Fig. 5
A new dose-response model for predicting the probability of
illness from Salmonella, based principally on data from disease
outbreaks (24)
The uncertainty bounds for the dose-response curves are superimposed on these curves.
The dose-response curves are generated from samples of outbreak data (each cross
represents the observed attack rate in one outbreak)
525
Rev. sci. tech. Off. int. Epiz., 23 (2)
– 202 cases from Danish pork
– 13 from imported pork
– 4 from turkeys
risk by a similar percentage. Thus, a large reduction in animal
prevalence, for example, from 20% down to 0.05% – a
reduction of 99.75% – would produce a 99.75% reduction in
the expected risk of human illness.
– 36 from broiler chickens
0.25
– 48 from imported beef
0.20
– slow cooling of food
– lack of refrigeration for several hours
– inadequate reheating before serving (24).
The FAO/WHO risk assessment (24) used the following
parameters in the production module of the exposure
assessment. This assessment predicted the percentage of
contaminated eggs among the population of all eggs
produced per unit of time:
a) the flock prevalence (uncertain scalar distribution with
parameter of 5%, 25% or 50%)
b) the percentage of infected hens within infected flocks
(log normal distribution; mean: 1.89%, standard deviation:
6.96%)
c) the fraction of eggs laid by infected hens that are
contaminated with S. enteritidis (Beta distributed uncertain
scalar, with parameter of alpha: 12, beta: 1109).
The dose of S. enteritidis consumed in a meal which
contains eggs depends on two factors, as follows:
– the amount of bacterial growth between the time the egg
is laid and when it is prepared
– how the egg is prepared and cooked.
The growth of S. enteritidis in contaminated eggs is a
function of storage time and temperature. The FAO/WHO
risk assessment includes the possibilities of yolkcontaminated eggs and the growth of S. enteritidis in eggs
before they are processed for egg products. These issues
have not previously been addressed in exposure
assessments of S. enteritidis in eggs. Yolk-contaminated
eggs might allow more rapid growth of S. enteritidis,
compared with eggs that are not yolk-contaminated (24).
The FAO/WHO exposure assessment for broilers estimated
the distribution of the average number of CFU of
100
1000
– cross-contamination
10
0.00
1
– inadequate cooking
0.1
0.05
0.000001
Important contributing factors in the development of
salmonellosis are, as follows:
0.01
0.10
0.001
– 271 from unknown sources (7).
0.15
0.0001
– 526 from travel associated sources
0.00001
– 74 from outbreaks
Relative frequency
– 17 from Danish beef
Average colony-forming units per cooked chicken serving
Fig. 6
An exposure assessment for broiler chickens, estimating the
distribution of the average number of colony-forming units of
Salmonella per serving for undercooked, contaminated chicken
Salmonella per serving for a contaminated chicken which is
then undercooked (Fig. 6). Note that, in Figure 6, the
interpretation of values of less than 1 CFU per serving is
1 CFU per multiple serving. For example, an average dose
of 0.01 bacterial cells per serving can be represented as one
serving out of 100 containing a single bacterial cell (24).
Risk characterisation
The international data, where available, indicate an
estimated human incidence of salmonellosis in 1997 of
14 to 120 cases per 100,000 (64). However, it is likely that
even these estimations reflect serious under-reporting.
The CDC estimate a total of 1.4 million human cases
(corresponding to an incidence of approximately 500 per
100,000) and 582 deaths in the USA annually (44).
In the FAO/WHO risk assessment, the probability of illness
(risk) was derived by combining the estimated number of
organisms ingested with information on the dose-response
relationship. The resulting risk characterisation enabled the
subsequent modification of the model parameters, so that
the efficacy of risk mitigation strategies that target those
parameters could be evaluated.
For broiler chickens, it was found that the relationship
between a reduction in the prevalence of Salmonellacontaminated chickens and the corresponding reduction in
the risk of human illness is one to one. That is, a percentage
change in animal prevalence will reduce the expected human
526
If management strategies are implemented that affect the
level of contamination, i.e. the numbers of Salmonella on
chickens, the impact on the risk of illness is estimated to be
greater than one to one. If the Salmonella cell numbers on
broiler chickens exiting the chill tank at the end of
processing are reduced by 40% on the non-log scale, this
reduces the expected risk of illness per serving by
approximately 65%.
It was also found that a small reduction in the frequency of
undercooking and the magnitude of the undercooking
event results in a marked decrease in the expected risk of
illness per serving. However, it is important to note that
altering cooking practices does not address the risk of
illness through cross-contamination. The strategy of
changing the cooking practices of the consumer must be
tempered by the fact that cross-contamination may, in fact,
be the predominant source of the risk of illness, and the
nature of cross-contamination in the home is still a highly
uncertain phenomenon (24).
The risk of human illness from S. enteritidis in eggs increases
as flock prevalence increases. However, uncertainty about
the predicted risk also increases as flock prevalence
increases. Reducing flock prevalence results in a directly
proportional reduction in human health risk (e.g. reducing
flock prevalence from 50% to 25% results in a halving of the
mean probability of illness per serving). Reducing prevalence
within infected flocks also results in a directly proportional
reduction in human health risk. For example, the risk of
illness per serving from eggs produced by a flock with a 1%
within-flock prevalence is one-tenth that of a flock with a
10% within-flock prevalence. Adjusting both egg storage
time and temperature profiles for eggs from production to
consumption was associated with significant effects on the
predicted risk of human illness (24).
Risk management
Appropriate risk management strategies for controlling
salmonellosis can be effectively implemented by the
appropriate authority(ies) of each country and should be
discussed in the national context. Each country can select
those risk management strategies along the entire food
production chain which are most appropriate to its
particular situation. What is feasible and highly effective
for one country might be quite unrealistic and/or
ineffective for another. The FAO/WHO Salmonella risk
assessment provides information that may be useful in
determining the impact of various intervention strategies
on disease risk from contaminated eggs and poultry (24).
Similar risk assessments covering other food groups will
reinforce the scientific basis for action.
Different countries have implemented different programmes
to lower the risk of salmonellosis. In Sweden, a compulsory
Rev. sci. tech. Off. int. Epiz., 23 (2)
programme was established to control Salmonella in poultry.
It involved the test screening and quarantine of grandparent
stock and pre-slaughter test screening of broilers. Disease
control measures on parent stock, hatcheries and layers
continue to be voluntary in Sweden, but mandatory testing
of layers during production and before slaughter has been
required since 1994 (47).
In Denmark, from 1988 to 2000, authorities initiated a series
of action plans to control human salmonellosis primarily
through initiatives on the farm. Following the peaks of
human salmonellosis caused by serotypes related to pigs
(1988), chicken (1993) and eggs (1997), such action plans
did succeed in reducing Salmonella prevalence at the farm
level and the resulting human disease burden (30). It is
interesting to note that measuring the success of these
measures was only possible through centrally managed
typing regimes (primarily phage typing) of strains from the
whole food chain and from human isolates, enabling a
‘pathogen-account’ system attributing the fraction of human
disease to foods (see further description below).
Potential intervention programmes for egg production which
have been theoretically evaluated in the FAO/WHO risk
assessment include ‘test and divert’ systems, vaccination of
flocks and refrigeration of eggs. Programmes to test and
divert animals which tested positive for the presence of
Salmonella three times (at the beginning of egg production,
four months later and just before flock depopulation),
administered to the entire population of egg production
flocks for four years, would reduce the risk of human illness
from shell eggs by more than 90%. Testing once a year for
four years would reduce the risk by over 70%. Vaccination
programmes are assumed to be capable of reducing the
frequency of occurrence of contaminated eggs by
approximately 75%. The effects of time and temperature
restrictions were evaluated assuming a flock prevalence of
25%. Restricting shelf-life to fewer than 14 days reduced the
predicted risk of illness per serving by a negligible amount
(~ 1%). However, keeping retail storage temperatures at no
more than 7.7°C reduced the risk of illness per serving by
about 60%. If shelf-life were reduced to 7 days, risk per
serving would also be reduced by about 60% (24).
When following the success of management programmes, it
is important to be able to separate salmonellosis cases
according to food source. One interesting new approach
involves attempting to link the fraction of human
salmonellosis cases to food commodities. This approach
compares the relative fractions of the total number of
laboratory-confirmed human cases caused by different
Salmonella serotypes and phage types against the
corresponding Salmonella types isolated in the various food
sources. It is also called a ‘pathogen account’ system (4).
Investigations into the epidemiology of Salmonella in the
USA used only serotyping but were still able to tentatively
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Rev. sci. tech. Off. int. Epiz., 23 (2)
link the outcomes of pathogen-reduction programmes for
meat, poultry and eggs to the serotype distributions in
humans (53). Other investigations found important
differences between the serotype distributions of
Salmonella isolates taken from food animals after slaughter
and the serotype distributions of isolates taken from people
in the USA (57).
Although this study could be said to raise questions about
raw animal products being the primary source for human
salmonellosis, the implications of differences in ecological
behaviour and/or in the virulence of different serotypes
could also be questioned. In addition, the importance of
the relative fractions of salmonellosis caused by a non-meat
or non-food source was not dealt with directly. In general
the use of new typing methodology to improve linkage
capacity is an important new scientific area. Using such
methods and linking data, by means of a more formal risk
assessment methodology, may enable the broadening of the
‘relative isolate fraction’ approach to other food-borne
pathogens as well, resulting in more efficient linkages
between foods and patients.
Toxoplasma gondii
Introduction
Toxoplasmosis is a highly prevalent disease worldwide
with many serious, long-term implications. It is caused by
the obligate intracellular parasite Toxoplasma gondii.
National seropositivity figures range from 16% in the
general population in the USA (36) to between 40% and
80% in women of child-bearing age in countries in Europe
and Africa (3, 22).
The WHO first recognised the importance of
toxoplasmosis at an expert meeting in 1968. Almost
twenty years later, another meeting was held to discuss the
public health implications of the disease (68). Yet today
toxoplasmosis remains prevalent worldwide, without a
current policy or active programme to manage this disease.
The human disease burden of toxoplasmosis, particularly
to foetuses and immuno-compromised people, is probably
significant.
Hazard identification and characterisation
The obligate intracellular parasite T. gondii mainly affects
the central nervous system. The definitive host is the cat
family Felidae, in whose intestine the parasite undergoes
the sexual part of its life cycle. The parasite is transmitted
to a wide range of intermediate hosts in birds and
mammals, including humans.
Congenital toxoplasmosis, which occurs when a woman
becomes infected shortly before or during pregnancy, leads
to such foetal symptoms as mental retardation, blindness,
cerebral palsy, stillbirth and spontaneous abortion (64). In
the
immuno-compromised,
symptoms
include
retinochoroiditis, heart problems, psychiatric problems
and encephalitis. Even normally healthy individuals may
be negatively affected. There may also be a link between
toxoplasmosis and brain function, with infected men
exhibiting lower IQs and less novelty-seeking behaviour
than do their healthy counterparts (64).
The public health implications are highly significant.
Between 2 and 4 of every 1,000 live births worldwide are
affected by congenital toxoplasmosis. Furthermore,
acquired toxoplasmosis is one of the principal
opportunistic diseases affecting people with the human
immunodeficiency virus (HIV) (65).
Exposure assessment
Humans can become infected by several different modes of
transmission. The primary means is probably through
uncooked or undercooked meat, although direct ingestion
of cat faecal material through contaminated drinking water
or soil can be alternative routes of infection. In developed
countries, the food route is thought to be the most
important and in fact, in the USA, some 50% of Toxoplasma
infections are estimated to be food-borne (44). In Europe,
a multi-centre case-control study encompassing Naples,
Lausanne, Copenhagen, Oslo, Brussels and Milan
estimated that 30% to 63% of infections were due to
undercooked meat consumption (19). Comparable data
from developing countries are generally not available, but
the significant increase in meat consumption in these
countries seems to indicate that this route of infection will
increase in importance in these regions.
The infection route starts when a cat is first infected and
begins shedding oocysts in its faeces. These sporulate
within one to five days, and remain infective for up to one
year in moist conditions, and an indefinite period of time
in uncooked meat. The oocysts can be ingested by pigs or
sheep, ultimately resulting in cysts in the muscle of these
animals. These cysts will then be present in the meat but
can be inactivated by either high or low temperatures.
Likewise, the sporozoites can be directly ingested by
humans who come into contact with contaminated soil.
Human infection thus follows one of several different
routes, as follows:
– maternal-foetal transmission after infection of the
mother
– consumption of uncooked or undercooked meat
or contaminated water
– ingestion of soil
– contact with infected domestic or feral cats.
528
Rev. sci. tech. Off. int. Epiz., 23 (2)
Risk characterisation
Risk management
Although it is estimated that perhaps 25% of the general
population carry the Toxoplasma parasite, few have
symptoms because the immune system usually keeps the
parasite from causing illness.
The economic burden of toxoplasmosis is likely to be very
high. One study in the USA estimated a cost of
US$7.7 billion per year, for congenital infections alone
(14). One of the most pressing issues when confronting
this disease is the lack of well-designed, controlled studies
which analyse the cost effectiveness of the various public
health measures implemented to control the disease. The
most effective measure is to prevent women acquiring the
disease during pregnancy by avoiding risk factors for
T. gondii infection. Health education may decrease the
incidence of toxoplasmosis during pregnancy by 60%.
Those at the highest risk from acquired toxoplasmosis are
those with a compromised immune system, such as
HIV-positive people, organ transplant recipients, or those
undergoing chemotherapy. The organisation UNAIDS gives
figures for the prevalence of toxoplasmosis among those who
are HIV-positive:
– 21% in the Côte d’Ivoire
– 14% to 34% in Brazil
– 17% in Mexico
– 2% in Thailand
– 11% in Zaire (65).
Moreover, AIDS patients with toxoplasmosis can show an
altered mental status in as many as 60% of cases (64). In the
era before highly active anti-retroviral therapy (HAART),
acute toxoplasmosis was a symptom of AIDS in up to 30%
of cases. The advent of HAART has lowered the numbers of
affected HIV-positive individuals, but this remains an area
of great concern (28).
Several estimates of the level of risk of congenital
toxoplasmosis are available. In the USA, there are estimated
to be between 1 in 10,000 and 10 in 10,000 cases of
congenital toxoplasmosis in the country each year, leading to
between 400 and 4,000 new cases (33). On the other hand,
a study in France indicated that 54% of pregnant women
were seropositive, leading to 6.6 babies per 1,000 births
being born with toxoplasmosis each year (3). A study in
Franceville, Gabon, reported that the risk for congenital
toxoplasmosis was 3.4 per 1,000 (48). If primary infection of
the mother occurs during pregnancy, there is a 40% chance
of foetal infection. The transmission rate and severity of
infection are related to the gestational age of the foetus at the
time of infection. The brain and retina are often affected, and
there can be a wide range of clinical disease.
Risk estimates for healthy individuals are not readily
available, but seropositivity figures in the general population,
mentioned in the introduction to this section above and
ranging from 16% to 80%, seem to indicate a relatively high
risk of infection. The geographical spread of incidence
estimates of several of the different clinical manifestations of
toxoplasmosis has been documented. Developing countries
often have significantly higher incidence levels. In one
specific study from the UK, the general estimated lifetime
risk of ocular symptoms in British-born individuals was
18 per 100,000. However, in the same study, people born in
West Africa had a 100-fold higher incidence of symptoms
than people born in Britain (27).
Screening programmes for pregnant women and neonates
do exist in some countries. Since 1976, France has
implemented a screening programme involving premarital,
pre-natal and post-natal screening, in conjunction with
educating pregnant women about the disease (33). When
a pregnant woman seroconverts, drug therapy with
spiramycin is recommended and, if the foetus exhibits
infection, pyrimethamine and sulfadiazine or sulfadioxine
may be considered (33).
Educating girls, women of child-bearing age, pregnant
women and the immuno-compromised about the dangers
of toxoplasmosis, as well as veterinarians and health-care
workers, is one of the most cost-effective means of
controlling the disease. Basic hygiene precautions, such as
thoroughly cooking meat, avoiding cat faeces and washing
hands, surfaces, and cooking implements, are simple ways
to avoid infection. Promoting the ‘Five keys to safer food’
WHO initiative (71) will also go a long way towards
preventing infection. These WHO recommendations are
simple rules which promote safer food handling and
preparation practices, as follows:
– keep hands, surfaces and utensils clean
– separate raw and cooked foods
– cook food thoroughly
– keep food at safe temperatures
– use safe water and raw materials.
In addition to these more general rules, some specific
recommendations should also be mentioned, as follows:
– do not allow cats on surfaces where food is prepared
– wash hands after handling cats and avoid kissing them
– cover outdoor sandboxes, as cats may use them as
litter trays.
529
Rev. sci. tech. Off. int. Epiz., 23 (2)
Toxi-infections alimentaires émergentes à caractère zoonotique
J. Schlundt, H. Toyofuku, J. Jansen & S.A. Herbst
Résumé
Les infections diarrhéiques, provoquées pour la plupart par des microorganismes pathogènes présents dans les aliments ou dans l’eau, constituent
une cause majeure de morbidité et de mortalité dans les pays les moins
développés. On estime qu’elles tuent chaque année près de 1,9 million de
personnes. Dans les pays développés, jusqu’à un tiers de la population serait
touché chaque année par une toxi-infection alimentaire microbiologique. La
majorité des micro-organismes pathogènes responsables de ce problème
sanitaire d’envergure sont désormais considérés comme des agents pathogènes
à caractère zoonotique. L’apparition de certains de ces agents au cours des
dernières années semble en nette augmentation.
Si les facteurs responsables de cette augmentation n’ont pas été étudiés de
façon approfondie, un lien est généralement établi avec l’évolution des systèmes
de production animale et de la chaîne de production alimentaire, notamment, qui
modifie le type d’exposition et de sensibilité au sein de la population humaine.
L’objet de cet article n’est pas d’offrir une analyse plus approfondie de ces
facteurs, mais de décrire succinctement cinq agents pathogènes émergents à
caractère zoonotique parmi les plus importants : Salmonella spp.,
Campylobacter spp., Escherichia coli entérohémorragique, Toxoplasma gondii et
Cryptosporidium parvum. Il ne vise pas une description exhaustive des
principaux agents pathogènes émergents à caractère zoonotique, mais propose
une synthèse de la situation au regard de ces agents pathogènes, les plus
importants sur le plan mondial. Chaque agent pathogène est décrit
conformément au nouveau système d’évaluation des risques microbiologiques
établi conjointement par l’Organisation des Nations unies pour l’alimentation et
l’agriculture (FAO) et l’Organisation Mondiale de la Santé (OMS), qui prévoit
l’identification et la caractérisation des dangers, l’évaluation de l’exposition et la
caractérisation du risque. Les auteurs présentent en outre un bref compte rendu
des actions entreprises en vue de réduire les risques, ainsi que des suggestions
en matière de gestion des risques pour certains des agents pathogènes
s’appuyant sur des évaluations approfondies réalisées par la FAO et l’OMS à
l’échelle internationale. Ils soulignent qu’en matière de prévention des toxiinfections alimentaires, la diminution durable du risque pour la santé humaine
passe obligatoirement par des programmes scientifiquement fondés de
réduction des agents pathogènes à certaines étapes pertinentes de la chaîne de
production alimentaire dans son ensemble, « de l’étable à la table ».
Mots-clés
Agent pathogène – Campylobacter – Cryptosporidium – Escherichia coli
entérohémorragique – Évaluation des risques microbiologiques – Salmonelle –
Toxi-infection alimentaire – Toxoplasma.
530
Rev. sci. tech. Off. int. Epiz., 23 (2)
Zoonosis emergentes transmitidas por vía alimentaria
J. Schlundt, H. Toyofuku, J. Jansen & S.A. Herbst
Resumen
Las enfermedades diarreicas, provocadas casi todas por patógenos
microbianos transmitidos por los alimentos o el agua, constituyen una de las
principales causas de morbilidad y mortalidad en los países menos
desarrollados y son responsables, según las estimaciones, de la muerte de
1,9 millones de personas al año. Incluso en los países desarrollados se calcula
que hasta un tercio de la población se ve afectado cada año por enfermedades
microbianas de transmisión alimentaria. Hoy se considera que los patógenos
causantes de esta importante morbilidad son en su mayoría patógenos
zoonóticos. De unos años a esta parte, algunos de ellos parecen presentarse
con una frecuencia sensiblemente mayor.
Aunque no se han estudiado a fondo los factores relacionados con ese aumento,
en general se piensa que los más importantes son la evolución de los sistemas
de producción animal y los cambios en la cadena de producción alimentaria,
factores ambos que alteran los patrones de exposición y sensibilidad de las
poblaciones humanas.
Los autores no pretenden analizar en detalle esos factores, sino describir
brevemente cinco de los principales patógenos zoonóticos emergentes que se
transmiten por vía alimentaria: Salmonella spp., Campylobacter spp., Escherichia
coli enterohemorrágica, Toxoplasma gondii y Cryptosporidium parvum. No se trata
pues de describir exhaustivamente todos los patógenos de ese tipo sino de
exponer a grandes líneas la situación actual con respecto a los mencionados
patógenos, que figuran entre los más importantes a escala mundial. Los autores
describen cada microorganismo con arreglo a un modelo de determinación del
riesgo microbiológico de la Organización de las Naciones Unidas para la
Agricultura y la Alimentación (FAO) y la Organización Mundial de la Salud (OMS),
que integra la identificación y caracterización de los peligros, la evaluación de
la exposición y la caracterización de los riesgos. Además, los autores dan
cuenta brevemente de una serie de iniciativas para tratar de reducir el riesgo, y
formulan propuestas para gestionar los riesgos derivados de algunos de los
patógenos a partir del modelo FAO-OMS. Por otro lado recalcan que, en lo que
concierne a las enfermedades prevenibles transmitidas por vía alimentaria, la
reducción duradera de los riesgos que presentan para la salud humana pasa
necesariamente por programas dotados de sólidos fundamentos científicos que
sirvan para reducir la presencia de patógenos en los puntos pertinentes de la
cadena de producción “del campo a la mesa”.
Palabras clave
Campylobacter – Cryptosporidium – Determinación del riesgo microbiológico –
Enfermedad transmitida por vía alimentaria – Escherichia coli enterohemorrágica –
Microorganismo patógeno – Salmonella – Toxoplasma.
Rev. sci. tech. Off. int. Epiz., 23 (2)
531
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