Have humans always been able to digest milk?
The ability to digest milk as adults (lactase persistence) evolved relatively recently in human history. Originally, like in most mammals, lactase declines after infancy.
Based on scientific evidence, around 7,000–10,000 years ago, in populations that practiced dairy farming, genetic mutations arose that allowed some adults to continue producing lactase; an advantage because milk provided a reliable source of nutrition, hydration, and calories.
Milk and dairy products have remained integral components of the global diet until now. In 2023, the EU's per capita dairy consumption was 52.81 kg, with raw milk production reaching 160.8 million tonnes (96% from cows).
Dairy can pose health risks, including foodborne illnesses. Given their widespread consumption, controlling dairy-borne illnesses is crucial.
As a highly nutritious medium, milk and its by-products are prone to bacterial contamination by spoilage and pathogenic organisms. Microbiological hazards constitute the highest risk in dairy products as they are encountered more frequently than chemical and physical hazards.
A variety of microorganisms are present in dairy products. The most common pathogens are Salmonella, Listeria monocytogenes, Staphylococcus aureus, Escherichia coli O157:H7, Yersinia enterocolitica, Bacillus cereus, Clostridium botulinum, Mycobacterium bovis, Brucella abortus, Brucella melitensis, Campylobacter jejuni and Coxiella burnetii.
Microbial Contamination in the Dairy Supply Chain
How does microbial load enter the dairy supply chain?
During primary production, the farm environment is a key source of foodborne pathogens. Microbial contamination can occur through sources such as feed, water, feces, bedding material, and soil. For example, pathogens that survive digestion (especially spore-forming ones) can spread via fecal matter, contaminating teats, and consequently, the milk.
Besides external contamination, teats can be colonized by microorganisms internally. Mastitis is an infection of the mammary gland, and it is a well-known problem at dairy farms. One control point is the use of veterinary drugs, but antibiotics can lead to antimicrobial resistance. Additionally, since many people are allergic to them (e.g., penicillin), milk must be tested for antibiotic residues.
During the processing stages, the milking equipment is a source of microbiological contamination. Most microorganisms, including pathogens, have the capacity to form biofilms.
Pasteurizing milk, along with a comprehensive food safety program (e.g., Good Agricultural Practices, HACCP), can significantly reduce or eliminate the risk of foodborne illness. However, consuming raw milk, inadequate or faulty pasteurization, or post-pasteurization contamination can still pose a risk of dairy-borne diseases.
Are there alternatives to the traditional safety measures?
Bacteriophages: A Natural Biocontrol Agent
Bacteriophages are viruses that infect bacteria. They have a head structure containing the DNA genome and a tail structure that allows them to specifically recognize their host.
Discovered in 1915, bacteriophages have been widely used in human and veterinary medicine to treat bacterial infections, such as chronic otitis and dental caries.
Bacteriophages are classified into two groups based on their life cycle:
- Temperate phages integrate their genomes into the host bacterium without causing cell death (lysogenic pathway).
- Lytic phages cause cell lysis, releasing new virus particles that can begin the cycle again on a newly found susceptible host (lytic pathway). Their capacity to kill the bacterial cell makes them an effective biocontrol tool.
In the dairy industry, which depends on the metabolic capabilities of lactic acid bacteria (LAB), bacteriophages were initially identified as a major cause of fermentation failure. However, improvements in the quality of fermented dairy products facilitated the recognition of bacteriophages' beneficial properties as biocontrol agents.
Advantages of Bacteriophages
- The most abundant biological entity on Earth (estimated population of 10^31 individuals), present in all environments. Isolated from raw products, processed food, fermented products, seafood, and water. Thus, they are inevitably consumed by humans on a daily basis.
- Harmless to humans, animals and plants, since they consist mostly of nucleic acids and proteins.
- Self-multiplying as long as there is still a host threshold present. Successful lytic infection results in the release of multiple phages. No need for multiple applications, which is ideal for sealed food products such as bottles of milk.
- Continuously adaptation to altered host systems. As bacteria develop, phages create defense mechanisms for their survival.
- Prolonged shelf life.
- Relatively cheap & easy to isolate.
- Preservation of food organoleptic properties.
- High specificity. Targeting only their specific host bacteria while leaving the remaining microbiota unharmed. Preferable over antibiotics and/or other chemical treatments, which can harm beneficial microbiota due to their broad antibacterial spectrum.
- Treatment of mastitis.
- Ability for application in every stage of the dairy processing chain, as they can generally withstand food processing stresses (including food physiochemical conditions).
Application of Bacteriophages in the Dairy Industry
For the protection against pathogens, bacteriophages can be applied:
- Directly in living animals during primary production to prevent animal illness and reduce pathogen carriage in the gastrointestinal tract. For instance, they can be administered orally or rectally to control E. coli in ruminants.
- On foods during industrial food processing. For example, mixing phages into raw milk.
Beyond biocontrol, bacteriophages can be exploited as:
- Biosanitizers for food contact surfaces. Having the ability to infect biofilms formed during processes like dairy fermentation.
- Biopreservators. Having the ability to act against psychrotrophs that produce heat-stable enzymes, which can alter milk product integrity and produce off-flavors, thus reducing shelf life.
- Biodetectors of pathogens, offering an alternative to the existing culture-based and time-consuming methods.
Commercial bacteriophage-based products
The EU has not yet established a specific regulatory framework for bacteriophages, which would allow Europe to take full advantage of their very promising application in food. Although EFSA has conducted some evaluations regarding bacteriophages, the EU tends to be more restrictive than the US.
Approvals for products are typically granted at the national level within EU member states rather than through a unified EU-wide clearance process.
Several commercial bacteriophage-based products are already approved by the USDA and FDA and are certified as Generally Recognized As Safe (GRAS).
These include products such as PhageGuard L (formerly Listex™), which targets Listeria monocytogenes, PhageGuard S for Salmonella, and PhageGuard E for E. coli by Micreos Food Safety B.V., as well as ListShield™, EcoShield™, and SalmoFresh™ by Intralytix.
Conclusion
Scientific studies demonstrate the efficacy of bacteriophages against milk-borne pathogens, making them a promising alternative.
However, the overall legal requirements for their use in food safety is still evolving. Regulatory agencies remain hesitant due to the lack of robust evidence from fully controlled and supervised clinical trials.
Future research is necessary and should prioritize large-scale trials, as well as a deeper understanding of bacteriophage-host interactions, phage resistance acquired by hosts, and the rate of elimination from the animal body. Additionally, precise control of procedures, concentrations, and application timing is crucial for optimization.
Lastly, educating farmers, producers, and the public on the benefits of phages is essential.
References
- Eurostat (2024) https://ec.europa.eu/eurostat/statistics-explained/index.php?title=Milk_and_milk_product_statistics#Milk_production
- FAO. Gateway to dairy production and products, Health Hazards. https://www.fao.org/dairy-production-products/products/health-hazards/en
- Hoque, M., Mondal, S. (2019). Safety of Milk and Dairy Products. In: R.L. Singh, S. Mondal (Eds), Food Safety and Human Health (pp 127-143), Academic Press. https://doi.org/10.1016/B978-0-12-816333-7.00005-9.
- Itan, Y., Powell, A., Beaumont, M.A., Burger, J., Thomas, M.G. (2009). The origins of lactase persistence in Europe. PLOS Computational Biology.
- Leonardi, M., Gerbault, P., Thomas, M.G., Burger, J. (2012). The evolution of lactase persistence in Europe. A synthesis of archaeological and genetic evidence. International Dairy Journal, 22 (2), 88-97.
- M. Shahbandeh (2024). Consumption of milk per capita in the EU-27 2019-2023. Statista. https://www.statista.com/statistics/1192244/europe-per-capita-milk-consumption/#statisticContainer
- O'Sullivan, L., Bolton, D., McAuliffe, O., Coffey, A. (2019). The use of bacteriophages to control and detect pathogens in the dairy industry. International Journal of Dairy Technology, 73 (1).
- Rogovski, P., Cadamuro, R.D., da Silva, R., de Souza, E.B., Bonatto, C., Viancelli, A., Michelon, W., Elmahdy, E.M., Treichel, H., Rodríguez-Lázaro, D., Fongaro, G. (2021). Uses of Bacteriophages as Bacterial Control Tools and Environmental Safety Indicators. Frontiers in Microbiology.
- Sillankorva, S.M., Oliveira, H., Azeredo, J. (2012). Bacteriophages and their role in food safety. International Journal of Microbiology.