Microbial food spoilage: A major concern for food business operators

‘Something is fishy’ is a widely used expression over a doubtful, suspicious situation, a good example of how mankind has taken advantage of microbial spoilage to assess the wholesomeness of a food product. The reduction of trimethylamine oxide to trimethylamine by bacteria associated primarily with the marine environment (e.g. Alteromonas and Vibrio) and animal intestines (Enterobacteriaceae) constitutes this major spoilage reaction during the storage of marine fish and typically identified ‘fishy’ as off note. The microbial alteration of fish can be therefore organoleptically identified by consumers, considering the food as suspicious for consumption1.

Spoilage of food involves any change which renders food unacceptable for human consumption and may result from a variety of causes, which include:

• Insect damage
• Physical injury due to freezing, drying, burning, pressure, radiation
• Activity of indigenous enzymes in plant and animal tissues
• Chemical changes not induced by microbial or naturally occurring enzymes. These changes usually involve O2 and light and other than microbial spoilage are the most common cause of spoilage e.g. oxidative rancidity of fats and oils and the discolouration of cured meats
• Growth and activity of microorganisms: bacteria, yeasts and moulds

Food unfit for consumption may not necessarily be spoiled and may contain a high number of food poisoning causing bacteria without presenting any ‘negative’ characteristics. Microbial deterioration of food is evidenced by alteration in the appearance (colour changes, pockets of gas / swelling), texture (soft and mushy), colour, odour and flavour or slime formation.

The numerous sources of microbial spoilage come from undesired yet ubiquitous micro-organisms which can originate from the natural habitat, e.g. soil, water, air, spoiled raw materials, biofilms on the surface of equipment, personal hygiene of food workers. Most foods serve as a good growth medium for many different microorganisms. Considering the variety of foods and the methods used for processing, it is apparent that practically all kinds of microorganisms are potential contaminants and can cause changes in appearance, flavour, odour and other qualities of foods. These degradation processes include putrefaction (proteolytic microorganisms), undesired fermentation (saccharolytic microorganisms) and rancidity (lipolytic microorganisms).

Definition

Microorganisms are commonly present in foods. Depending on their characteristics and growth potential, they can play different roles: commensals (neither metabolic nor adverse health effects), probiotics (health benefit on the host), pathogens (adverse health effects on the host), food cultures (technological benefit), and spoilers (deleterious metabolic activity on the food product).

Food microbiology focuses on the relationship of habitat to occurrence of microorganisms, the effect of environment on growth of various microorganisms in food, the microbiology of food spoilage and food manufacture, the physical, chemical, and biological destruction of microorganisms in foods, the microbiological examination of foodstuffs, and public health and sanitation bacteriology.

Food spoilage is a metabolic process that causes foods to be undesirable or unacceptable for human consumption due to changes in sensory characteristics. Spoiled foods may be safe to eat, i.e. they may not cause illness because there are no pathogens or toxins present, but changes in texture, smell, taste, or appearance cause them to be rejected.

The real economic cost of food spoilage is difficult to estimate. It is generally considered that circa 30 per cent of manufactured food product is spoiled, microbial food spoilage being the major cause9.

From the EU 2020 Resource Efficiency Flagship presenting a strategic framework for a more sustainable and efficient use of natural resources, it is estimated that every person wastes about 179 kilograms of food a year. In total, this is about 89 million tonnes per year. Food waste is expected to rise in Europe to about 126 million tonnes7.

Food spoilage is wasteful and costly, can adversely affect the economy and can erode consumer confidence. Product compliance also means unspoiled products at the retailer level and during their shelf life. A good knowledge of the food product characteristics and its microbial ecology is therefore a priority for food business operators.

Common groups of foods spoilers

Sources of microbial spoilage are either ubiquitous microorganisms from soil, water and air or special sources of contamination, depending on the ecological microbial niche from spoiled raw materials, food waste, biofilm on the surface of equipment and personal hygiene from food workers or consumers.

Since spoilage depends both on the food matrix and the microorganism of concern, assessing the variety of microbial food spoilage is like opening Pandora’s Box. A comprehensive approach is quite unfeasible though we tried to make a first small attempt in Table 3. The major groups are shortly described hereafter.

Table 3: Examples of different food spoilage (far from being comprehensive)

Lactic acid bacteria

Under the globalised term LAB, the following genera are most commonly included: Lactobacillus, Weisella, Leuconostoc, Lactococcus, Pediococcus, Streptococcus, Enterococcus.

Lactic acid bacteria are widely distributed in various ecological niches and are generally used for the metabolic activity of organic acid production in dairy products and on sourdough. Yet this activity can be harmful (acetic acid, gas blowing, post acidification) to food matrices (e.g. processed cheese) or beverages (fruit juices, beer)11.

Acetic acid bacteria

Acetic acid bacteria (AAB) are ubiquitous organisms that are well adapted to sugar and ethanol rich environments. Twelve genera are recognised and belong to the family Acetobacteraceae, the Alphaproteobacteria: Acetobacter, Gluconobacter, Acidomonas, Gluconacetobacter, Asaia, Kozakia, Swamina – thania, Saccharibacter, Neoasaia, Granulibacter, Tanticharoenia and Ameyamaea. Isolation, purification, identification and preservation of AAB are very difficult. Wine is at most risk of spoilage during production and the presence of these strictly aerobic bacteria in grapes must and, during wine maturation, can be controlled by eliminating, or at least limiting oxygen, an essential growth factor2.

Filamentous fungi, yeasts

Filamentous fungi cause the main ‘visual’ aspect of spoilage through a mouldy appearance, and can sometimes have toxicogenic properties depending on the species. Fungal spoilage may be characterised by highly visible, often pigmented growth, slime, fermentation of sugars to form acid, gas or alcohol or off odours/off flavours. Though they can spoil various types of food products, they are most commonly found in fruits and cereals.

Yeasts8 typically spoil high acid, low pH, high sugar (more than 10 per cent), high salt (more than five per cent) or weak organic acid (sorbic, acetic, benzoic acid) preserved products. Therefore, fruit and fruit-based products, sugar syrups, alcoholic or carbonated beverages, salad dressings and other acid sauces, dairy products and fermented foods are often associated with yeast spoilage.

Gram negative bacteria:

Enterobacteriaceae, Pseudomonadaceae

Gram negative rod-shaped bacteria may grow at chill temperatures and have been shown to contribute to the spoilage of chilled red meat, cured meats, poultry, fish, shellfish, milk and dairy products, e.g. Acinetobacter, Aeromonas, Pseudomonas (most common), Alcaligenes, Alteromonas, Flavobacterium, Moraxella and Archromobacter. Vibrio spp. are halophilic and therefore may cause spoilage of sea fish and cured meats. Overall, the group is not heat-resistant and can be readily removed by mild thermal treatments.

Enterobacteriaceae are generally slowergrowing at chilled temperatures and become more significant if the temperature rises above 5°C (dominating between 8 – 15°C). Many strains are psychrotrophic and have been isolated from vacuum packed meats, poultry, cured meats, milk, dairy and egg products.

Spore forming bacteria

Alicyclobacillus spp.12, Bacillus spp. and Clostridium spp. are of particular significance due to their ability to produce heat-resistant spores which can survive many heating / pasteurisation processes and germinate under suitable conditions and grow in foods4. They are therefore most commonly seen in the spoilage of canned foods.

Factors interacting with microbial food spoilage

A variety of factors determine whether microbial growth will preserve or spoil foods. Intrinsic or food related parameters are inherent to the food product; they are the chemical and physical characteristics of food. Extrinsic or environ – mental, external factors are the properties of storage environments which affect both food as well as microorganisms. Implicit factors are the result of mutual interactions in mixed microbial populations. Such factors are summarised in Table 1.

Table 1: Factors interacting with microbial food spoilage

Growth hurdles according to the food properties

In most foods, preservative factors work in combination and play a decisive role for both microbial quality and safety. These preservative factors are called hurdles, and the so-called hurdle effect concept was introduced in the late 1970s as an illustration for the complex interactions of several inhibitory factors in the preservation of foods. Using a ranking basis on the food properties (i.e. intrinsic factors), food matrices can be classified as proposed in Table 2.

Table 2: Growth hurdles accordnig to the food properties

Predicting bacterial growth and shelf life appraisal

Predictive modelling does not solely address pathogenic microorganisms. Based on the same approach, models for microbial spoilage of different foods and for spoilage by specific organisms examine the effects of the preservative factors to predict the spoilage process. Based on and validated with actual experimental data, these models can provide useful information for product development and modification, shelf-life estimates, processing requirements and quality assurance programs.

Food spoilage is a complex process involving a variety of organisms, food matrices, food preservatives and additives. Depending on their objective, models are constructed to focus on probability of growth/no growth, time required to initiate growth, growth rate or survival of spoilage organisms under a particular set of parameters. Inactivation and destruction of microbes exposed to different preservatives or preservation techniques can also be modelled. However, models cannot incorporate every factor that may affect the spoilage process and processors should validate models for their own products to account for different variables3,10.

Detection of microbial spoilage

Microbial spoilage can be detected by organoleptic, microbiological and chemical investigations.

Biogenic amines from proteolysis of the food matrix provoke typical off note odours and flavours that are easily recognised by consumers to consider a food product unfit for consumption. These molecules can be a topic of safety concern on certain fermented food products5.

Spoiled foods usually have microbial counts over 107 CFU/g from a quite limited number of species (except for fermented foods)6. Therefore, only qualitative investigations are conducted generally on spoiled products. To assess the incipient spoilage population before it becomes organoleptically detectable, conventional microbiological testing such as total mesophilic count, thermoresistant count or yeast and moulds count are sufficient.

A chemical method can also be used when the spoilage of food is already characterised, such as pH measurements for acid producers or specific detection of spoilage metabolites, e.g. with Fourier transform infrared spectroscopy. Risk management options In order to control or at least minimise contamination, a risk management from farm to fork is mandatory, with actions that should be focused on:

• GMP, good manufacturing practices and good management processes
• GHP, good hygienic practices, acceptable sanitary practices
• Rapid movement of food through processing plant
• Well-tested preservation procedures
• Microbial specifications of raw materials and end products
• Good hygienic design following EHEDG Guidelines

Though HACCP plans apply to food safety, the same approach is to be conducted for the microbial quality versus microbial food spoilers.

The food process can be modified as following to reduce potential of microbial spoilage:

• Removal of microorganisms: partial or complete through heat inactivation, physical filtration, irradiation
• Minimising microbial growth potential through refrigeration, freezing, lyophilisation and inhibitory compounds (e.g. chemically with preservatives, biologically with bacteriocins)

One might be aware of relevant changes in the food process and its implications on spoilage. For example, a change of suppliers for raw materials with a natural occurring flora can have no consequence on the safety of the product but major ones on its quality. On the other hand, improving safety by a new bactericidal treatment can modify the ecological niche and therefore the possibility of spoilage, both type of and microorganisms of concern. The shelf life of a food product therefore needs continuous monitoring to verify that GMP/GHP does not vary from initial validation.

References

1. Al Bulushi, I., Poole, S., Deeth, H.C., Dykes, G.A., 2009. Biogenic amines in fish: roles in intoxication, spoilage, and nitrosamine formation–a review. Crit Rev Food Sci Nutr. 49(4):369-77
2. Bartowsky, E.J., Henschke, P.A., 2008. Acetic acid bacteria spoilage of bottled red wine — a review. Int J Food Microbiol 125(1):60-70
3. Beaufort, A., Cornu, M., Bergis, H., Lardeux, A-L., Lombard, B., 2008. Technical Guidance Document on Shelf-life Studies for Listeria monocytogenes in Readyto- eat Foods. Version 2. http://ec.europa.eu/food/ food/biosafety/salmonella/docs/shelflife_listeria_mo nocytogenes_en.pdf
4. Brown, K.L., 2000. Control of bacterial spores. Br Med Bull 56(1):158-71
5. EFSA Panel on Biological Hazards (BIOHAZ), 2011. Scientific Opinion on Scientific Opinion on risk based control of biogenic amine formation in fermented foods. EFSA Journal 9(10):2393
6. Ellis, D.I., Goodacre, R., 2006. Quantitative detection and identification methods for microbial spoilage, p. 3–27. In Blackburn C.W. (ed.), Food Spoilage Microorganisms. Wood Head Publishing CRC Press
7. EUROPA, European Commission, DG Health and Consumers, Overview, Food and Feed Safety, Environmental Sustainability of the Food Chain. http://ec.europa.eu/food/food/sustainability/ index_en.htm
8. Fleet, G.H., 2007. Yeasts in foods and beverages: impact on product quality and safety. Curr Opin Biotechnol. 18(2):170-5
9. Gram, L., Ravn, L., Rasch, M., Bruhn, J.B., Christensen, A.B., Givskov, M., 2002. Food spoilage—interactions between food spoilage bacteria. Int J Food Microbiol 78:79–97.
10. NACMCF, 2010. Parameters for Determining Inoculated Pack/Challenge Study Protocols. J Food Prot 73(1) 140-202
11. Sakamoto, k., Konings, W.N., 2003. Beer spoilage bacteria and hop resistance. Int J Food Microbiol. 89(2- 3):105-24
12. Smit, Y., Cameron, M., Venter, P., Witthuhn, R.C., 2011. Alicyclobacillus spoilage and isolation–a review. Food Microbiol 28(3):331-49

About the authors

François Bourdichon and Katia Rouzeau work within the Food Safety Microbiology Group, Quality and Safety Department of Nestlé Research Centre in Switzerland. They are in charge of microbial risk assessment and technical assistances for the Nestlé Group. They are also delegates of Nestlé and Switzerland in external bodies such as ILSI Europe and FIL-IDF.