This article features otherwise unpublished food safety management data held by BRCGS and Safefood 360° which, combined with real-time events, provides an unparalleled view of current and emerging issues and trends in the food safety industry.

 

Enteric bacteria reside in the intestines of humans and animals and form a major part of the gut microflora or microbiome that include bacteria, viruses, fungi and protozoa. The gut microbiome is recognised as having an important and positive effect on health but a number of enteric microorganisms are pathogenic and can be harmful. This article will focus on a group of enteric bacterial pathogens that are commonly associated with foodborne disease i.e. Salmonella species (spp.), Escherichia coli (E. coli), Shigella spp., Yersinia spp., Campylobacter spp., and Vibrio spp. Other enteric pathogens such as Clostridium difficle are clinically significant in human disease but are generally not considered foodborne enteric bacterial pathogens.

Controlling enteric pathogens requires an understanding of the organisms, the way they are spread, how they respond in food and to its processing and how they cause disease. The potential to cause illness in human populations is as much about the condition of the person who is exposed to the organism and the food in which it is consumed as it is about the organisms themselves. So, let’s explore a bit about each of these.

 

The history

Enteric bacterial pathogens have been around for some time with cholera-like illnesses being described in texts from India in the 5th century B.C. and, in Greece, by Hippocrates in the 4th century B.C. with the first pandemic emerging from the Ganges delta in India in 1817, spread by contaminated rice. For those interested in nomenclature, bacteria are often named after the person who discovered them, the place they were discovered or from the Greek or Latin word for their morphology. For example, Salmonella Poona is named after D. E. Salmon who first isolated the bacterium from a pig intestine in 1884 and the location where this isolate caused an early outbreak. Escherichia coli takes its genus name from Theodor Escherich, a pioneering Bavarian paediatrician who first isolated it from infant faecal samples in 1885, and its species name, ‘coli’, from the colon, the organism’s natural habitat. Yersinia spp. are named after Alexandre Yersin, a Swiss bacteriologist who first isolated an infamous member of the genus, Yersinia pestis, the cause of the plague, in 1894. Yersinia pestis is not an enteric bacterial pathogen but is in the same genus as Yersinia enterocolitica, that is a recognised foodborne pathogen. To finish the naming conventions, Shigella spp. are named after the Japanese bacteriologist Kiyoshi Shiga who isolated the dysentery bacillus in 1898, Vibrio spp. take their name from the latin “vibrare” which means to vibrate or move rapidly, describing their rapid motility and, finally, Campylobacter spp. are named after the Greek words for curved “kampylos” and rod “baktron” that describes the shape of their cells.

 

The organisms and how they are spread

Enteric bacterial pathogens are infectious organisms, in contrast to toxigenic bacteria that predominantly cause illness through the production of pre-formed toxins in a food e.g. Staphylococcus aureus, Clostridium botulinum, Bacillus cereus, etc. An infectious pathogen must by alive in the food consumed in order to cause an illness. The illness, in the case of enteric pathogens, will usually start with multiplication in the small intestine of the host. Multiplication is often also associated with the local production of toxins by the enteric bacteria. Unlike many microorganisms that we consume in food, enteric pathogens are able to survive the harsh conditions that they are exposed to after ingestion including lysozyme in the saliva, gastric acids and bile. The infectious dose of enteric pathogens i.e. the levels required to cause infection can vary markedly as it is affected by host immunity, the food vehicle and the state of the organism. Under the right conditions, many enteric bacterial pathogens can cause infection from a small number of cells e.g. 10-100. However, it is recognised that different levels of a pathogen can be associated with varying probabilities of infection, often referred to as the dose response, with higher doses being associated with the higher likelihood of infection.

Enteric bacterial pathogens reside in the intestines of humans and animals and therefore faecal contamination of a food from human or animal wastes is the conventional means by which the organisms are spread. This can be through direct transfer e.g. animal faeces to raw milk during milking, to raw chicken or other raw meats during slaughter and processing, through the application of animal wastes to growing crops, the deposition of faeces by birds / reptiles / vermin and through the transfer of human waste from an infected food handler to the food, etc. However, in many cases indirect means of transfer occurs through other vehicles. For example, water may be contaminated with human or animal wastes and be used for agricultural crops or may contaminate crops during periods of flooding. Animals and pests, that may not be the primary source of the organism, may transfer contamination from such sources to foods and contamination from raw foods may be transferred to other raw or ready to eat foods by direct contact, through indirect contact of common transport, storage or processing vessels or utensils or via food handlers. Due to the widespread contamination of environmental sources such as water and land with human and animal faeces, some enteric pathogens colonise environmental niches and consequently cross contamination from general environmental sources may introduce the pathogen to the food rather than direct faecal contamination. Although enteric bacterial pathogens can be associated with many foods and environments, there are some particular associations between certain pathogens and food types.

  • Campylobacter spp., pathogenic to humans, including jejuni and C. coli can be found in high numbers in the faeces of poultry, pigs, cattle and other animal species and consequently are associated with foodborne illness from raw animal products i.e. chicken, turkey, duck, pork, raw milk. Water contaminated with faeces has also been implicated in many outbreaks.
  • Yersinia include two species that are mostly associated with foodborne illness, Y. enterocolitica and Y. pseudotuberculosis with pigs being the primary source and the consumption of raw or undercooked pork being the main cause.
  • Vibrio include many species, with the most notable being V. cholerae, the causative organism of the severe enteric disease cholera, spread by faecally contaminated water and foods and with an estimated 1-4 million cases and 21 – 143 000 deaths per year. Many of the other Vibrio species causing foodborne disease e.g. V. parahaemolyticus, V. alginolyticus, etc. are not spread like conventional enteric pathogens such as V. cholerae although most do still result in symptoms of enteric disease including nausea, vomiting, stomach cramps and diarrhoea. Some species such as Vibrio vulnificus can also cause severe wound infections such as necrotising fasciitis (“flesh eating bacteria”). These other Vibrio spp. live naturally in certain warm, coastal waters including salt and brackish water environments. Consequently, they tend to be particularly associated with the consumption of raw or lightly cooked seafood such as oysters, crab and other seafood.
  • Shigella spp. infections (shigellosis or bacterial dysentery) are spread via human faeces to food, water or from person to person via direct contact or contact with food or common contact surfaces. The four Shigella (S. boydii, S. sonnei, S. flexneri and S. dysenteriae) can cause severe illness resulting in diarrhoea that can be bloody and the organism spreads rapidly in schools, institutions and settings where maintaining high standards of sanitation may be more difficult. Foods particularly associated with outbreaks due to Shigella spp. include salad vegetables where the contamination source is generally the irrigation water and also those ready to eat foods that are extensively handled during their preparation.
  • Escherichia coli include many strains that harmlessly reside in the intestines of humans and animals. However, some strains can cause illness with the most serious being those that produce a potent toxin, the Shiga toxin-producing coli (STEC). STEC are especially associated with cattle faeces although other ruminants such as sheep, goats and deer have also been found to carry and shed the organism. Foods most at risk of contamination include those vulnerable to contamination with cattle faeces, in particular. Outbreaks have most often been associated with raw or undercooked ground beef products such as burgers, raw / unpasteurised milk and raw milk cheeses and salad vegetables.
  • Salmonella species are perhaps the group of enteric bacterial pathogens where illness and outbreaks are associated with the consumption of the widest range of foods. With the exception of Salmonella Typhi and Paratyphi, the two strains associated with typhoid and paratyphoid fever, respectively, where transmission is exclusively through human faecal contamination of food, water or direct person to person spread, the non-typhoidal Salmonella (of which there are over 2500 serotypes / serovars) have their origin in human and animal faeces. However, in the case of non-typhoidal Salmonella spp., the organisms are now so widely distributed in the environment that it is often not possible to trace a contamination event directly to faecal contamination as this is often several stages removed from the vehicle transmitting the organism to the food. Nevertheless, products derived from animals that harbour Salmonella spp. such as eggs, poultry meat, pork, raw milk and raw milk products are frequently implicated in outbreaks of salmonellosis together with salad vegetables exposed to animal waste products. But the list of food outbreaks extends far and wide including herbs and spices, nuts and seeds, cookie dough, melons, peanut butter, fish, sprouts, mushrooms, tahini, etc.

 

How they cause disease and typical symptoms

Enteric bacterial pathogens cause disease by multiplying in the intestine and causing physical disruption of intestinal structures such as villi, sometimes accompanied by the production of toxins. The villi are responsible for absorption of water and associated nutrients and therefore any disruption can lead to poor water uptake from food resulting in a watery bowel movement, that we know as diarrhoea. In some enteric infections, the damage to the villi can be so pronounced that the blood vessels lining the villi rupture, releasing blood into the stool, observed as bloody diarrhoea. Enteric bacterial pathogens may also produce toxins in the intestine that are taken up and cause effects in the intestine or elsewhere in the body. For example, Vibrio cholerae produces a toxin in the small intestine that stimulates the release of electrolytes and water by intestinal cells into the intestine resulting in profuse watery diarrhoea. In some cases, enteric bacterial pathogens enter the blood system in what is described as bacteraemia (bacteria in the blood) where they can either cause an infection of the blood supply (septicaemia) or in a localised tissue or organ e.g. haemolytic uraemic syndrome (kidney).

Typical symptoms of enteric bacterial infection are a combined result of the organism, its toxin and the host response to these and include including nausea, abdominal pain, vomiting, diarrhoea, bloody diarrhoea, fatigue, malaise, elevated body temperature / fever and flu-like symptoms. Symptoms of infection (see Appendix 5 in the Bad Bug Book) usually occur within 18-36 hours although this can range from 12 hours to several days. In the majority of cases, illness is self-limiting and patients make a full recovery. However, infection with some enteric bacterial pathogens can result in death and long-term morbidity. This can be particularly pronounced in vulnerable groups such as the elderly, children and those with depressed immune responses such as immunocompromised. Notable examples include dysentery from Shigella dysenteriae and cholera from Vibrio cholerae, both of which cause many deaths each year in less well developed countries where the disease causes dehydration and electrolyte loss that cannot be sufficiently replaced. Shiga toxin-producing E. coli (STEC) produce a potent toxin that can result in kidney failure and / or the long term requirement for dialysis, Even Salmonella spp., and Campylobacter spp., infection can result in death, especially in vulnerable individuals and campylobacteriosis can result in long term adverse health consequences such as reactive arthritis and Guillain-Barré syndrome, a degenerative neurological conditions leading to paralysis. 

 

Response to food and food processing

A key element in the control of enteric foodborne pathogens is through the application of food formulation or processing to reduce the organisms to a safe level or eliminate them completely. Intrinsic factors of the food such as pH, water activity and preservatives (salt, acids, etc) are generally used to control the growth of microorganisms (inhibition) but many of them also have a lethal effect on the organism (destruction). Understanding the factors affecting the growth and survival of an organism in a food is critical if intrinsic factors are to be relied upon to achieve safety in relation to enteric bacterial pathogens. Each organism and even strains of specific organisms can respond differently to intrinsic factors and it is important to account for these differences when formulating foods to control these pathogens. For example, some strains of Salmonella spp., and STEC are especially acid tolerant and where acidity is relied upon to destroy the pathogen such as in the case of raw, fermented / dried meats or fermented vegetables it is important to understand the conditions necessary for die off of the organism during fermentation and / or drying. Many enteric bacterial pathogens can survive for long periods in dry and frozen food and this should not be relied upon to eliminate the organisms or reduce them to safe levels. In general, as the presence of any viable enteric bacterial pathogen in a ready to eat food is considered potentially unsafe, foods that are at risk of contamination with these organisms are usually treated or processed in such a way as to reduce them to a safe level or eliminate them completely. The most common treatment for eliminating enteric bacterial pathogens is heat processing as none of these bacteria produce spores and this has been a widely adopted process technology for centuries. Although recommended processes vary throughout the world, a temperature / time combination of 70°C for 2 minutes or equivalent processing has been used for raw meats and other foods to deliver safe ready to eat products. Such processes deliver reductions of enteric bacterial pathogens in excess of 6 orders of magnitude or 6 log units. It is important to note that the effect of heat on a microorganism is subject to the presence of water in the food and low moisture foods require higher heat processes to destroy microorganisms. Conversely, the presence of inhibitory substances such as acids and salts can enhance the effect of heat. In addition to the effect of intrinsic properties of the food on the survival of enteric bacterial pathogens, some strains are inherently more heat resistant.

Many foods cannot tolerate heat processing such as fruits and vegetable (and remain organoleptically acceptable) and therefore other approaches are usually adopted to reduce the risk from contaminating enteric bacterial pathogens. This includes washing, spraying or fogging with a variety of disinfectants including chlorine, sodium hypochlorite, chlorine dioxide, hydrogen peroxide, ozone and many others. In general, these techniques tend to achieve only a moderate reduction in contamination with levels usually reducing by 1-2 orders of magnitude. They therefore need to go alongside other controls to minimise the risk of occurrence of the organism in the raw material such as good agricultural practices. Alternative methods of processing are also effective in destroying enteric bacterial pathogens including high pressure processing, cold plasma treatment, and irradiation.

 

Strategies for preventing illness from enteric foodborne bacterial pathogens

Understanding enteric bacterial pathogens, how they spread and cause illness and how they are affected by the composition and processing of food provides us with the means to effectively manage them to ensure they do not present a risk to the end consumer of a food. Essentially this consists of two main strategies, namely, preventing the organisms from contaminating a food or, if they are present, apply a process to eliminate them. For many foods derived from raw ingredients that are frequently contaminated with enteric bacterial pathogens such as raw meat, poultry, eggs, etc., an assumption is made that the organisms will be present and therefore a process must be applied to destroy the organism or reduce them sufficiently to ensure they does not present a risk in the finished product. The processing techniques have already been described (see above). For other foods, including those that have received a processing step to eliminate the organisms, it is essential that contamination is not introduced or re-introduced. This is achieved through recognised good agricultural practices (GAP) for fresh produce including fruits and salad vegetables and through the application of good hygienic practices (GHP) in the handling and processing of foods. There are many excellent texts on GAP and GHP with a recent publication from the European Union being a good reference text for the former (GAP) and the Codex General Principles of Food Hygiene (CXC 1-1969) being the obvious and most relevant text for GHP. The fundamental principles of Codex underpin all of the voluntary third-party assurance schemes for food safety management such as the BRCGS Global Food Safety Standard and certification to these standards provide independent verification that a food business has an effective food safety management programme. The use of software such as Safefood 360° facilitates a structured approach to the development and management of the food safety management programme.

Given the breadth of different enteric bacterial pathogens, it is not possible to detail other specific measures that need to be adopted for control of each of these in the very many different foodstuffs that they may present a risk to but links already provided on each of the organisms will give you a place to start your journey in understanding and controlling these fascinating foodborne hazards.

 

Summary

I hope I have given you a bit of an insight into the control of foodborne enteric bacterial pathogens and whetted your appetite to delve deeper into the organisms and their effective management.

 

Author

 

Alec Kyriakides

BRCGS International Advisory Board Chair

Independent Food Safety Consultant