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Journal of Family Medicine and Disease Prevention

DOI: 10.23937/2469-5793/1510035

Microbiological Safety of Food, Particularly for Vulnerable People

Barbara M Lund*

Institute of Food Research, Norwich Research Park, UK

*Corresponding author: Barbara M Lund, Institute of Food Research, Norwich Research Park, Colney, Norwich, NR4 7UA, UK, E-mail:
J Fam Med Dis Prev, JFMDP-2-035, (Volume 2, Issue 2), Review Article; ISSN: 2469-5793
Received: April 07, 2016 | Accepted: June 22, 2016 | Published: June 25, 2016
Citation: Lund BM (2016) Microbiological Safety of Food, Particularly for Vulnerable People. J Fam Med Dis Prev 2:035. 10.23937/2469-5793/1510035
Copyright: © 2016 Lund BM. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


Foodborne illness affects about one in six Americans each year. Certain groups of people are particularly susceptible to foodborne illness, these include the very young, the elderly, pregnant women and people whose immune system is suppressed by disease or medication. These groups are most likely to incur infection and to suffer severe consequences. Major foodborne pathogens and foods that are particularly associated with hazards are outlined. Fa ctors leading to outbreaks are described and illustrated with examples of outbreaks. Prevention of transmission of foodborne pathogens involves use in the supply of food of a system based on the Hazard Analysis Critical Control Point System (HACCP) and prerequisite programs, and the selection of lower-risk foods in place of higher-risk foods for vulnerable people.


Salmonella, Toxoplasma, Listeria, Campylobacter, Norovirus, HACCP, Low-microbial diet, Neutropenic diet


HACCP: Hazard Analysis Critical Control Point, STEC: Shiga Toxin-Producing Escherichia coli

Incidence of Foodborne Disease, and Major Foodborne Pathogens

It is estimated that each year one in 6 Americans becomes ill as a result of consuming contaminated food or beverages [1]. Most of these illnesses are caused by pathogenic microorganisms including bacteria, viruses and parasites. A wide range of pathogens can cause foodborne disease and result in different types of symptom. The annual incidence of foodborne illness caused by 31 foodborne pathogens in the USA was estimated by Scallan et al. [2]; results for major pathogens are shown in table 1. The main causes of deaths were non-typhoidal Salmonella (NTS), Toxoplasma gondii and Listeria monocytogenes. Reports from Canada and Europe show a majority of cases caused by Campylobacter, Clostridium perfringens, norovirus, non-typhoidal salmonella (NTS), and shiga-toxin-producing Escherichia coli (STEC), and a high case-fatality due to the parasite T. gondii and to L.monocytogenes [3]. An assessment was made in the US of loss of quality-adjusted life years (QALY), taking into account long-term sequelae, for 14 foodborne pathogens [4]; results for the five pathogens that contribute 90% of the total QALY loss are shown in table 2. In their list of major foodborne pathogens the FDA includes the following organisms that cause fewer cases of illness but can have very serious consequences, particularly in vulnerable people, Cryptosporidium, Vibrio vulnificus and in infants Cronobacteria [5]. The present paper will discuss the importance and consequences of foodborne infection in vulnerable people and methods to prevent infection, using examples involving the foodborne pathogens responsible, in industrialized countries, for the greatest burden of disease in terms of loss of QALY and number of cases of illness.

Table 1: Estimated annual number of domestically acquired foodborne illnesses, hospitalizations and deaths caused by major foodborne pathogens in the USA. Data from [2]. View Table 1

Table 2: Estimates of quality-adjusted life year (QALY) loss and cost of illness for 5 main foodborne pathogens Data from [4]. View Table 2

Vulnerable People and their Susceptibility to Foodborne Pathogens

In many cases previously healthy people recover well from foodborne illness, but in some cases the consequences are serious and long-term. In vulnerable people the consequences are liable to be much more serious, and to result from infection by lower numbers of a pathogen [6]. Many vulnerable people are those who have an immune system that is suppressed to some extent; these include the very young, the elderly, pregnant women and people whose immune system is suppressed by disease or by medication. It has been estimated that approximately 20% of the population in the USA has a compromised immune system [7,8].

Host factors that increase the risk of foodborne and waterborne infection and the severity of the disease are shown in table 3.

Table 3: Host factors that increase the risk of foodborne and waterborne infection and/or the severity of the disease. Modified from [9]. View Table 3

Many enteric pathogens show higher rates of reported infection in children < 5 years old than in older children and adults [10]. Scallan et al. [11] studied the effect of 4 major bacterial enteric pathogens causing foodborne illness in older adults, compared with the effect in other age groups (Table 4).The highest recorded rate of infection with NTS, Campylobacter and E.coli O157 was in the group aged < 5 years, while the highest rate of infection with Listeria was in adults aged > 65 years. For infection with each of the four pathogens the percentage of patients who died was higher in people aged > 65 than in the other age groups.After allowing for underreporting it was estimated that the highest number of deaths in the > 65 age group were caused by NTS and L.monocytogenes.

Table 4: Average annual rate of laboratory-confirmed infections and deaths, due to 4 major foodborne pathogensin the US1996-2012. Data from [11]. View Table 4

Non-typhoidal Salmonella spp. cause much more severe illness, including invasive and focal suppurative disease, in immune compromised than in immunocompetent adults [12,13]. Adults with diabetes, long-term steroid medication, haematological malignancy, advanced or disseminated solid cancers, autoimmune disease, liver disease, renal transplantation and people taking immunosuppressive drugs are susceptible to NTS bacteraemia. Patients with haematological malignancy were reported to be at increased risk of Salmonella or Campylobacter infection compared with people without malignancy [14], and in England and Wales in 2007 older persons (≥ 60 years, who are liable to be affected by chronic conditions) were the age group most at risk of campylobacteriosis [15]. Invasive disease due to Campylobacter spp. is reported to be rare, but is more frequent in people with comorbidities and immune-compromising conditions [16].

The relative susceptibilities of different subpopulations to L.monocytogenes are shown in table 5; data from the USA indicated that persons aged over 60 years were 2.6 times more susceptible than the general healthy population while perinatals were 14 times more susceptible.In pregnant women infection usually causes a mild, flu-like illness, but the bacterium can cross the placenta and infect the foetus, leading to abortion, stillbirth, or delivery of an acutely ill infant. Subsequent reports have confirmed the increasing risk with increasing age over 60 and the marked susceptibility associated with various types of cancer, particularly those associated with the blood [18-21]. The high level of risk in patients with AIDS (Table 5) has reduced considerably in some countries in recent years, probably as a result of the availability of antiviral therapy for HIV infection [20]. Use of cytotoxic drugs, drugs affecting the immune response, and corticosteroids resulted in particular susceptibility to listeriosis [22]. Risk factors for death as a result of listeriosis included particular malignancies, alcoholism, cardiovascular disease, increasing age, and treatment to reduce gastric secretion; some previous workers also identified steroid medications and kidney disease/renal failure as independently associated with mortality [23].

Table 5: Relative susceptibilities of different sub-populations to listeriosis, based on French epidemiological data [17]. View Table 5

Infection by the parasite T.gondii can lead to serious illness, particularly in pregnant women and their infants and in people with impaired immunity [24,25]. Following infection, pregnant women may not show symptoms of infection, but the organism may spread to the foetus and can lead to miscarriage, stillbirth, and severe disease in the newborne or development of disease later in infancy, childhood or adolescence [26].

In immunocompetent people infection with T.gondii is generally asymptomatic, but can result in lymphadenopathy, ocular symptoms (chorioretinitis) or occasionally effects on the central nervous system; following infection, the organism can persist as cysts in various tissues of the body, particularly in the brain, retina and muscles. In immunocompromised people toxoplasmosis can result from primary infection or from reactivation of latent cysts, which can occur if there is a decline in the person’s immune system, particularly in AIDS, transplant and cancer patients [27-29] and can lead to ocular, cerebral or disseminated toxoplasmosis. Toxoplasmosis is a significant cause of eye disease in the USA [30]. Cats are the definitive host of T.gondii and can shed infective oocysts in the environment; these oocysts may result in infection of other animals. Human infection can result from consumption of water or vegetables contaminated by oocysts from cat faeces, or from consumption of undercooked meat or raw milk of infected animals. Because of the risk of transfer of oocysts from cat faeces, pregnant women and immunocompromised people are advised to wear gloves when gardening or handling soil or sand from sand boxes and to wash their hands thoroughly afterwards [24]. If possible, these groups should also avoid changing cat litter boxes, which should be changed daily, and cats should not be fed raw meat. In view of the potential risk posed by latent cysts in immunocompetent people if they become immunocompromised, the advice given above is appropriate for the general population. There are differences in the detailed advice given in European countries and the USA [25].

Foodborne infection with norovirus can result in extensive person-to-person spread of the virus. In immunocompetent people norovirus infection usually results in gastroenteritis lasting 24-48 h and is self-limiting, but the virus can be shed in the faeces for 20-40 days [31]. In immunocompromised people the gastroenteritis can be chronic and can persist for weeks or years. Prolonged norovirus-associated diarrhoea can result in malnutrition, dehydration, and altered intestinal mucosal barrier [32].

Main Foods Associated with Hazards

Based on estimated disease burden, in terms of loss of Quality-Adjusted Life Years (QALY) and cost of illness the top 50 pathogen-food combinations in the USA were ranked by Batz et al. [33], the top 14 of which are shown in table 6. An estimate of the main pathogen-food combinations, based on studies in the literature, is shown in table 7. Foods of animal origin are associated with the major proportion of cases of foodborne illness, but foods of non-animal origin are also associated with many outbreaks and cases. In the USA top-ranking risk groups of non-animal foods were listed as: (1) E.coli O157:H7 and leafy greens, (2) Salmonella and tomatoes, (3) Salmonella and leafy greens, Salmonella and melons, (4) E.coli O157:H7 and crucifers and melons [35]. In the European Union the top-ranking risk groups were listed as: (1) Salmonella and leafy greens eaten raw, (2) Salmonella and bulb and stem vegetables, Salmonella and tomatoes, Salmonella and melons, and pathogenic E.coli and fresh pods, legumes or grains [36].

Table 6: Ranking of disease burden for major pathogen-food combinations in the USA based on loss of QALY and cost of illness. Data from [33]. View Table 6

Table 7: Foods associated with disease caused by major foodborne pathogens. Information derived from studies in several countries. Data from [34]. View Table 7

Main Factors Leading to Transmission of Foodborne Pathogens

Five main factors leading to transmission of foodborne pathogens have been listed by the FDA [37].
These include:
- Food from unsafe sources
- Inadequate cooking
- Improper holding temperatures
- Contaminated equipment
- Poor personal hygiene

Examples of outbreaks that have resulted from such factors are shown table 8.

Table 8: Examples of outbreaks of foodborne disease. View Table 8

Many cases of toxoplasmosis appear to be sporadic, and outbreaks are rarely detected because many individuals affected show few or no immediate symptoms.A number of outbreaks, mainly affecting a few people, were described by Smith [26]. These were associated mainly with consumption of raw meat or raw goat milk.

Prevention of Foodborne Disease

Detailed advice on the provision of safe food in retail and in food service is given in the FDA Food Code [37].

Control of food production

The FDA Food Code [37] recommends, and European regulations [63] require that food business operators should put in place, implement and maintain a permanent procedure or procedures based on hazard analysis and critical control point principles (HACCP). The HACCP plan is designed to provide safety from biological, chemical and physical hazards, and includes the following actions:
(1) Identify any hazards (2) Identify the critical control points (CCPs); - the points at which control is needed to prevent, remove or reduce a hazard in the process
(3) Set critical limits to assure that the operation is under control at a particular control point
(4) Establish and implement monitoring systems at control points
(5) Take corrective action when critical limits are not met
(6) Have checks in place to verify that the system is working
(7) Keep records

This applies to meals supplied in hospitals and institutions as well as other food businesses. In order for a HACCP system to be effective, prerequisite programs must be in place to control the basic operational and hygiene conditions (including Good Manufacturing Practice) within an operation [37].

Avoid food from unsafe sources

The FDA Food Code specifies that food should be obtained from sources that comply with the law [37]. Food prepared in a private home may not be offered for human consumption in a food establishment.Specifications are included regarding the source and labelling of specific types of food. Special requirements are included for foods prepared in an establishment that serves a highly susceptible population.

Ensure adequate cooking

Conditions advised for cooking foods (Table 9) are based on a requirement to inactivate vegetative microbial pathogens including Campylobacter spp, STEC, NTS and L.monocytogenes, the most heat-resistant of this group.

Table 9: Temperatures and times advised for thorough cooking of animal foods. A food thermometer should be used to check the internal temperature reached throughout the food. View Table 9

Ensure control of holding temperature

Clostridium spp., including Clostridium perfringens, form spores that are heat-resistant and are not inactivated by cooking. In order to prevent foodborne illness due to C.perfringens meals, particularly meat dishes that are not eaten immediately but are prepared in advance, should be cooled within two hours from 57°C to 21°C and within 6 hours from 57°C to 5°C [37]. These meals should not be allowed to remain at temperatures between 12°C and 50°C, which can allow the surviving spores of C.perfringens to germinate and the vegetative bacteria to multiply to numbers that can cause food-poisoning after consumption of the meal. Meals that are prepared and stored should be reheated to at least 74°C for 15 sec before consumption [37].

Freezing can inactivate tissue cysts of T.gondii in meat. Tissue cysts in pork were usually inactivated by freezing at an internal temperature of -12.37°C, but survived freezing at -6.7°C for up to 11 days [68].

Chilled foods should be maintained in a refrigerator at 5°Cor lower, to reduce growth of food-poisoning bacteria and maintain the safety and quality of the food. L. monocytogenes can grow slowly at temperatures as low as 3°-5°C.

Prevent contamination of equipment

Food contact surfaces, including meat slicers, should be cleaned thoroughly. Raw foods and ready-to-eat foods should be well-separated. Separate equipment and utensils should be used for raw and cooked food.

Maintain good personal hygiene

For food handlers, personal cleanliness and good hygienic practices are essential. In the section on Employee Health the FDA Food Code [37] gives full information on the conditions that food employees must meet to avoid transmitting foodborne disease. It lists symptoms that a food handler must report to the person in charge and conditions that require workers to be restricted or excluded from working in a food establishment. Restriction means that a food employee’s activities are limited to prevent the risk of transmission of disease via food i.e. there is no contact with exposed food or food-contact materials. Exclusion means that a food employee is not permitted to work or enter a food establishment as an employee.

A food employee should be excluded from a food establishment if the person shows symptoms of vomiting or diarrhoea caused by an infection, or has symptoms diagnosed as due to an infection with norovirus, Shigella spp., NTS or STEC. A person diagnosed with hepatitis A infection within 14 days from the onset of any illness symptoms, or within 7 days of the onset of jaundice or who has not developed symptoms should also be excluded. A food employee who is diagnosed with an infection with S.Typhi or reports a previous infection with S.Typhi within the past 3 months should be excluded.

A person who is diagnosed with an infection with norovirus, Shigella spp., STEC, but is asymptomatic, should be excluded from working in a food establishment serving highly susceptible people, or restricted from working in a food establishment not serving a highly susceptible population. A person diagnosed with non typhoidal Salmonella infection and is asymptomatic should be restricted from working in a food establishment that serves a highly susceptible population, or in an establishment not serving a highly susceptible population.

A person ill with symptoms of acute onset of sore throat and fever should be excluded from working in a food establishment serving a highly susceptible population, or restricted from working in a food establishment not serving a highly susceptible population. A food employee with a skin lesion containing pus that is open and not properly covered should be restricted from working as a food employee.

A person who has been exposed to a foodborne outbreak or case involving norovirus, (in the past 48 hours), STEC or Shigella (within the past 3 days), S.Typhi (within the past 14 days) or Hepatitis A virus (in the past 30 days) should be restricted from working in a food establishment that serves a highly susceptible population.

The conditions in which restricted or excluded persons are again allowed to work in a food establishment [1] not serving a highly susceptible populationor [2] serving a highlysusceptible population, are outlined in the US Food Code [7]. Comparable guidance for food handlers is published in the UK [69].

Selection of Lower-Risk Foods

The FDA has issued guidance for people at risk of foodborne illness, including Older Adults, People with Cancer, and people with Diabetes, people with HIV/AIDS, Pregnant Women, and Transplant Recipients [5]. In each case the advice includes a similar section on the selection of lower-risk foods (Table 10). More detailed ‘low risk diets’ (‘low-microbial diets’ or ‘neutropenic diets’) are advised by many hospitals and other organizations, for highly immunosuppressed people [70-77].

Table 10: Food safety for people with cancer [5]. View Table 10

These diets aim to omit higher-risk foods, identified as potential sources of organisms that cause infection especially in immunocompromised people, and substitute lower-risk (safer) foods. In relation to listeriosis, high-risk foods are defined as foods with the following properties: (i) have the potential for contamination with L.monocytogenes (ii) support the growth of L.monocytogenes to high numbers (iii) are ready to eat (iv) require refrigeration, and (v) are stored for an extended period of time [78].

There have been several criticisms of low-microbial diets; from a review of randomized, controlled trials comparing the effect of use of a low-microbial diet with a control diet on infection rate, it was concluded that the three main studies had serious methodological limitations, and no definitive conclusions could be drawn [79]. There are differences in detail between some of thelow-microbial diets, but the essential feature of avoiding foods that are known to have the potential to transmit foodborne pathogens, and substituting safer foods providing similar nutritive value, is clearly important to ensure that vulnerable people do not suffer severe consequences as a result of foodborne infection.

More general agreement on such recommendations would be valuable, and as new information about the microbiological safety of foods becomes available such diets may need to be modified.


Up to 20% of people in the US, UK and other industrialised countries are particularly vulnerable to foodborne disease. Procedures are available that are designed to minimize this risk. These procedures need to be recognised universally and to be implemented. According to Silk et al. [80] "evidence for the problem of unsafe food preparation and service for immune compromised and elderly patients is not only widespread, but also underestimated and can be expected to grow". They stressed that professional organisations should promote, and large healthcare systems should establish, policies to prepare safe food for immune compromised patients, and not serve them higher-risk foods. The same care is needed in the provision of food for immune compromised persons in the community.


I am grateful to Dr A.C. Baird-Parker and to Professor M.W. Peck for helpful comments during the writing of this paper.

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