Inactivation of foodborne pathogens by the synergistic combinations of food processing technologies and food‐grade compounds

There is a need to develop food processing technologies with enhanced antimicrobial capacity against foodborne pathogens. While considering the challenges of adequate inactivation of pathogenic microorganisms in different food matrices, the emerging technologies are also expected to be sustainable and have a minimum impact on food quality and nutrients. Synergistic combinations of food processing technologies and food‐grade compounds have a great potential to address these needs. During these combined treatments, food processes directly or indirectly interact with added chemicals, intensifying the overall antimicrobial effect. This review provides an overview of the combinations of different thermal or nonthermal processes with a variety of food‐grade compounds that show synergistic antimicrobial effect against pathogenic microorganisms in foods and model systems. Further, we summarize the underlying mechanisms for representative combined treatments that are responsible for the enhanced microbial inactivation. Finally, regulatory issues and challenges for further development and technical transfer of these new approaches at the industrial level are also discussed.     

Principles and recent applications of novel non-thermal processing technologies for the fish industry—a review

Thermal treatment is a traditional method for food processing, which can kill microorganisms but also lead to physicochemical and sensory quality damage, especially to temperature-sensitive foods. Nowadays consumers’ increasing interest in microbial safety products with premium appearance, flavor, great nutritional value and extended shelf-life has promoted the development of emerging non-thermal food processing technologies as alternative or substitution to traditional thermal methods. Fish is an important and world-favored food but has a short shelf-life due to its extremely perishable characteristic, and the microbial spoilage and oxidative process happen rapidly just from the moment of capture, making it dependent heavily on post-harvest preservation. The applications of novel non-thermal food processing technologies, including high pressure processing (HPP), ultrasound (US), pulsed electric fields (PEF), pulsed light (PL), cold plasma (CP) and ozone can extend the shelf-life by microbial inactivation and also keep good sensory quality attributes of fish, which is of high interest for the fish industry. This review presents the principles, developments of emerging non-thermal food processing technologies, and also their applications in fish industry, with the main focus on microbial inactivation and sensory quality. The promising results showed great potential to keep microbial safety while maintaining organoleptic attributes of fish products. What’s more, the strengths and weaknesses of these technologies are also discussed. The combination of different food processing technologies or with advanced packaging methods can improve antimicrobial efficacy while not significantly affect other quality properties under optimized treatment.     

Fruit juice sonication: Implications on food safety and physicochemical and nutritional properties

Over the last years, consumers are increasingly demanding for nutritious, healthy and fresh-like food products, with high organoleptic quality. Nowadays, emerging non-thermal technologies have raised great interest as a viable alternative to the conventional thermal methods, since they have minimal impact on sensorial and nutritional properties of fresh foods. Ultrasound (US) is one of these promising non-conventional processing technologies and it is especially suitable for preservation of fluid foods. US may be used alone or in combination with other preservation techniques, such as mild heat temperatures, high pressures and antimicrobials. Besides, data on inactivation of food microorganisms by US alone are scarce, because the effects of US are usually not severe enough for a sufficient lethal effect. Since many studies on this subject have been published in the last two decades, this review intends to analyze the main effects of US on microbiological, nutritional and physicochemical parameters of fluid foods. While some general trends can be observed, the effects of US are usually highly variable, not only according to treatment duration and intensity, but also according to the food matrix, suggesting that each matrix should be studied and evaluated separately. Generally, the impact of US on food matrices is minimal, unless longer treatment times and higher amplitudes are applied. Other parameters such as the specific resistance of the microbial strain play also a role.     

Advances in innovative processing technologies for microbial inactivation and enhancement of food safety – pulsed electric field and low-temperature plasma

The need for enhancing microbial food safety and quality, without compromising the nutritional, functional and sensory characteristics of foods, has created an increasing world-wide interest in low-temperature innovative processes for food preservation. In contrast, to the traditional thermal processes, these emerging technologies are predominantly reliant on physical processes, including high hydrostatic pressures, pulsed electric fields and low-temperature plasmas that inactivate microorganisms at ambient or moderately elevated temperatures and short treatment times. The current review presents the latest developments in the two most recent of these technologies, pulsed electric field and low-temperature plasma treatments for food preservation and disinfection of food contact surfaces.     

Reaction Kinetics at High Pressure and Temperature: Effects on Milk Flavor Volatiles and on Chemical Compounds with Nutritional and Safety Importance in Several Foods

Consumers demand, in addition to excellent eating quality, high standards of safety and nutrition in ready-to-eat food. This requires a continuous improvement in conventional processing technologies and the development of new alternatives. Prevailing technologies such as thermal processing can cause extensive and undesirable chemical changes in food composition while minimal processing strategies cannot eliminate all microbial pathogens. This review focuses on pressure-assisted thermal processing, a new alternative for shelf-stable foods. Its implementation requires an analysis of reaction kinetics at high pressure and elevated temperature. Acceleration of the inactivation of bacterial spores by the synergistic effect of pressure and temperature is expected to allow processing at lower temperature, shorter process time, or a combination of both. Therefore, thermal degradation of quality is expected to be lower than that of conventional thermal processes. However, few studies have focused on the effect of the conditions required for the inactivation of bacterial spores on the kinetics of chemical reactions degrading food quality, particularly at the high temperatures required for the processing of low-acid foods.     

Applications of novel processing technologies to enhance the safety and bioactivity of milk

Bioactive compounds in food can have high impacts on human health, such as antioxidant, antithrombotic, antitumor, and anti-inflammatory activities. However, many of them are sensitive to thermal treatments incurred during processing, which can reduce their availability and activity. Milk, including ovine, caprine, bovine, and human is a rich source of bioactive compounds, including immunoglobulins, vitamins, and amino acids. However, processing by various novel thermal and non-thermal technologies has different levels of impacts on these compounds, according to the studies reported in the literature, predominantly in the last 10 years. The reported effect of these technologies either covers microbial inactivation or the bioactive composition; however, there is a lack of comprehensive compilation of studies that compare the effect of these technologies on bioactive compounds in milk (especially, caprine and ovine) to microbial inactivation at similar settings. This research gap makes it challenging to conclude on the specific processing parameters that could be optimized to achieve targets of microbial safety and nutritional quality at the same time. This review covers the effect of a wide range of thermal and non-thermal processing technologies including high-pressure processing, pressure-assisted thermal sterilization, pulsed-electric field treatment, cold plasma, microwave-assisted thermal sterilization, ultra-high-pressure homogenization, ultrasonication, irradiation on the bioactive compounds as well as on microbial inactivation in milk. Although a combination of more than one technology could improve the reduction of bacterial contaminants to meet the required food safety standards and retain bioactive compounds, there is still scope for research on these hurdle approaches to simultaneously achieve food safety and bioactivity targets.     

Application of ohmic heating for the inactivation of microbiological hazards in food products

Ohmic heating has long been used to inactivate pathogens in food products. Several research investigations on the use of ohmic heating technology in the inactivation of microbial hazards in food products are discussed in this review. These studies are discussed under the following sub-headings: (a) inactivation of microbiological hazards, (b) in combination treatments with other sanitizing technologies, and (c) mathematical modeling, all of which are of long-standing interest. In this review, we evaluate ohmic heating as a rapid and volumetric heating process that inactivates microbiological hazards in food products. We also examine ohmic heating-based combination treatments as promising methods to maximize microbial inactivation efficacy and minimize the quality deterioration of food products. We first highlight the fact that most researchers had an interest in the inactivation of vegetative pathogens, whereas only a few focused on the inactivation of bacterial spores. In general, significantly higher treatment conditions were needed to inactivate bacterial spores (>95°C) than vegetative pathogens (>50°C). Studies on the inactivation of viral pathogens by ohmic heating are limited, and further research is needed in this field. In the first part of this review, the nonthermal effects of ohmic heating are also discussed, which is a popular topic in the food industry. Cumulatively, research suggests that that these nonthermal effects are dependent on the treatment conditions and the electrical conductivity of different food samples. Therefore, we suggest that focus should be on the thermal rather than the nonthermal effects of ohmic heating when considering the application of this technology to inactivate pathogens. Finally, we introduced combination technology based on ohmic heating and mathematical modeling, which are of interest recently.     

Trends in microbial control techniques for poultry products

Fresh poultry meat and poultry products are highly perishable foods and high potential sources of human infection due to the presence of several foodborne pathogens. Focusing on the microbial control of poultry products, the food industry generally implements numerous preventive measures based on the Hazard Analysis and Critical Control Points (HACCP) food safety management system certification together with technological steps, such as refrigeration coupled to modified atmosphere packaging that are able to control identified potential microbial hazards during food processing. However, in recent years, to meet the demand of consumers for minimally processed, high-quality, and additive-free foods, technologies are emerging associated with nonthermal microbial inactivation, such as high hydrostatic pressure, irradiation, and natural alternatives, such as biopreservation or the incorporation of natural preservatives in packaging materials. These technologies are discussed throughout this article, emphasizing their pros and cons regarding the control of poultry microbiota and their effects on poultry sensory properties. The discussion for each of the preservation techniques mentioned will be provided with as much detail as the data and studies provided in the literature for poultry meat and products allow. These new approaches, on their own, have proved to be effective against a wide range of microorganisms in poultry meat. However, since some of these emergent technologies still do not have full consumer's acceptability and, taking into consideration the hurdle technology concept for poultry processing, it is suggested that they will be used as combined treatments or, more frequently, in combination with modified atmosphere packaging.     

The inactivation of Salmonella by cold atmospheric plasma treatment

The need to fulfill consumer demand for fresh products without compromising microbial food safety and quality has increased the interest of the food industry in low-temperature innovative processes for food preservation. Compared to thermal processing, these emerging technologies rely on physical processes, such as high hydrostatic pressure, ionizing radiation, ultrasonication, pulsed electric fields, ultraviolet radiation and cold plasmas that are able to inactivate microorganisms at ambient or sublethal temperatures. This latter treatment is one of the more promising food preservation technologies. In this review we survey the main factors affecting the sensitivity and resistance of Salmonella to cold atmospheric gas plasmas. A more complete understanding of the factors involved in inactivation by this emerging technology will enhance its implementation in food preservation.     

Biological Aspects in Food Preservation by Ultraviolet Light: a Review

The potential to commercialize nonthermal ultraviolet (UV) light technologies as new methods for preserving food products has caught the attention of a food industry that wishes to fulfill consumers' demands for fresh products. Numerous investigations have demonstrated UV light's ability to inactivate a wide range of microorganisms. However, the lack of UV sensitivity data from pathogenic and spoilage bacteria is evident. In addition, the main factors associated with UV light in terms of microbial lethality remain unclear. This review surveys critical factors (process, microbial, and environmental parameters) that determine UV microbial resistance and assess the effects of such factors on the inactivation mechanism and repair pathway efficiency. The effects of some of these factors, such as prior sublethal stresses and post-recovery conditions of UV treatments, may extensively improve the damage repair capacity and thus microbial survivability. Further research is needed to establish adequate control measures pre- and post-UV treatments. Furthermore, the possibility of combining UV light with conventional preservatives and other nonthermal technologies was assessed. The combination of UV light with mild heating or oxidant compounds could offer promising treatments to enhance the safety and stability of minimally processed foods.     

Quality-Related Enzymes in Plant-Based Products: Effects of Novel Food-Processing Technologies Part 3: Ultrasonic Processing

High-power ultrasound is a versatile technology which can potentially be used in many food processing applications including food preservation. This is part 2 of a series of review articles dealing with the effectiveness of nonthermal food processing technologies in food preservation focusing on their effect on enzymes. Typically, ultrasound treatment alone does not efficiently cause microbial or enzyme inactivation sufficient for food preservation. However, combined with mild heat with or without elevated pressure (P ≤ 500 kPa), ultrasound can effectively inactivate enzymes and microorganisms. Synergistic effects between ultrasound and mild heat have been reported for the inactivation of both enzymes and microorganisms. The application of ultrasound has been shown to enhance the rate of inactivation of quality degrading enzymes including pectin methylesterase (PME), polygalacturonase (PG), peroxidase (POD), polyphenol oxidase (PPO), and lipoxygenase (LOX) at mild temperature by up to 400 times. Moreover, ultrasound enables the inactivation of relatively heat-resistant enzymes such as tomato PG1 and thermostable orange PME at mild temperature conditions. The extent to which ultrasound enhances the inactivation rate depends on the type of enzyme, the medium in which the enzyme is suspended, and the processing condition including frequency, ultrasonic intensity, temperature, and pressure. The physical and chemical effects of cavitation are considered to be responsible for the ultrasound-induced inactivation of enzymes, although the dominant mechanism depends on the structure of the enzyme.     

Nonthermal preservation of foods using combined processing techniques

In the last 2 decades, consumer demand for fresher, higher quality, and safer food has promoted research on nonthermal methods of food preservation for the inactivation of microorganisms and enzymes as an alternative to thermal processes. However, the high resistance of certain enzymes and microorganisms to nonthermal processes, especially bacterial spores, limit their application. To expand the use of nonthermal processes in the food industry, combinations of these technologies with traditional or emerging food preservation techniques are being studied. The use of nonthermal processes in combination with other preservation technologies presents a number of potential benefits to food preservation. The purpose of this article is to review some successful combinations of different nonthermal technologies, such as high hydrostatic pressure, ultrasound, pulsed electric fields, and irradiation, with traditional or emerging food preservation technologies.     

非热杀菌技术杀灭食品中芽孢效能及机理研究进展

传统热杀菌会对食品品质产生不利影响,造成食品颜色变化、产生异味、营养损失等不良后果;非热杀菌技术是食品工业新型加工技术,处理过程中可以保持相对较低的温度,对食品的色、香、味以及营养成分影响较小;同时有利于保持食品中各种功能成分的生理活性,可以满足消费者对高品质食品的要求。芽孢在加工过程中抗性强,在食品中萌发和生长的潜力较大,因此,利用低热或非热灭菌技术对芽孢进行灭活是当前食品工业面临的严峻挑战和重要课题。本文综述现有非热杀菌技术（如高静压技术、高压CO2技术、低温等离子体技术、紫外辐射技术、高压脉冲电场技术等）独立处理或与其他处理技术相结合对芽孢灭活的效果及其机理,着重讨论其在食品行业中的应用以及芽孢灭活的分子机制,以期为生产安全食品、减少不同种类食品中微生物污染提供解决方案。     

Enhancing Food Processing by Pulsed and High Voltage Electric Fields: Principles and Applications

ABSTRACT

Improvements in living standards result in a growing demand for food with high quality attributes including freshness, nutrition and safety. However, current industrial processing methods rely on traditional thermal and chemical methods, such as sterilization and solvent extraction, which could induce negative effects on food quality and safety. The electric fields (EFs) involving pulsed electric fields (PEFs) and high voltage electric fields (HVEFs) have been studied and developed for assisting and enhancing various food processes. In this review, the principles and applications of pulsed and high voltage electric fields are described in details for a range of food processes, including microbial inactivation, component extraction, and winemaking, thawing and drying, freezing and enzymatic inactivation. Moreover, the advantages and limitations of electric field related technologies are discussed to foresee future developments in the food industry.

This review demonstrates that electric field technology has a great potential to enhance food processing by supplementing or replacing the conventional methods employed in different food manufacturing processes. Successful industrial applications of electric field treatments have been achieved in some areas such as microbial inactivation and extraction. However, investigations of HVEFs are still in an early stage and translating the technology into industrial applications need further research efforts.     

Enhanced bacterial inactivation in apple juice by synergistic interactions between phenolic acids and mild food processing technologies

This study demonstrated an innovative processing approach based on synergistic antimicrobial activity of two phenolic acids with mild thermal and non-thermal processing technologies. The two selected model phenolic acids were gallic acid (GA; 10 mM) and ferulic acid (FA; 1 mM). The processing technologies evaluated for processing of a model clarified apple juice were UV-A light, mild heat (55 °C) and moderate pressure (250 MPa), with processing times ranging from 1 to 30 min. The results demonstrated that combinations of selected phenolic acids and a mild physical processing were able to lower E. coli O157:H7 and Listeria innocua counts from 6-log CFU mL⁻¹ to below the detection limit of 1-log CFU mL⁻¹. Bacterial inactivation was significantly enhanced by the combination of UV-A light processing and FA, where 10 min of treatment enhanced bacterial inactivation by 5-log as compared to light processing alone, which presented no bacterial inactivation. In contrast, the combination of GA and mild-temperature thermal processing (55 °C) or mild-levels of high-pressure processing (250 MPa), enhanced bacterial inactivation by 4-log as compared to the physical treatments alone, which presented only 1-log of inactivation. The influence of these synergistic combinations on bacterial membrane damage was assessed by selective plating technique under osmotic pressure. Furthermore, the total intracellular thiol content was also measured to assess for thiol oxidation. Overall, the results demonstrated enhanced bacterial inactivation based on synergistic interactions of selected phenolic acids with both mild-thermal and non-thermal technologies in a model food system and illustrate potential to create diversity of novel antimicrobial strategies for food processing.Industrial relevanceThis study showed that the presence of naturally-based compounds can significantly reduce intensity levels of physical processing required to inactivate model gram-positive and gram-negative bacteria in apple juice. In this study two phenolic acids, ferulic acid and gallic acids were selected as these compounds are naturally present in many fruits and other food products including grains. Furthermore, the levels of these natural phenolic acids used in this study are comparable to the levels naturally present in some of the food materials.     

Dairy foods and novel thermal and non-thermal processing: A bibliometric analysis

Processing dairy products by conventional methods, such as pasteurization, can induce chemical reactions and physicochemical alterations, compromising nutritional and sensory quality. Thus, there is a growing worldwide demand for studies related to emerging processing technologies. This study aims to describe trends related to dairy processing through the application of emerging technologies. In this sense, articles published in this area of research in the last decade were retrieved from scientific databases, and their findings were analyzed through a bibliometric study. Reviews and original articles expressed 40 and 60% of publications, respectively, and novel thermal and non-thermal processing studies showed multidisciplinary approaches. Ohmic heating and microwave heating were the most discussed novel thermal technologies in the processing of dairy products. Among non-thermal technologies, there was a more significant trend in studies on ultrasound, high hydrostatic pressure, and pulsed electric fields. The impact of the application of novel food technologies concerning quality, safety, and energy efficiency compared to traditional methods and the influence of critical operating conditions for process control were the most studied areas. Furthermore, the impact of novel non-thermal food processing technologies from the consumer's point of view is emerging. These results can be used for future innovations by the dairy industry.Industrial relevanceDairy foods are important food matrices considering a nutritional and functional point of view and recommended in a regular diet for consumers of all ages. Therefore, a bibliometric analysis was performed considering dairy foods and novel thermal and non-thermal processing. A higher number of publications considering non-thermal technologies was reported, highlighting the need for food processing without applying high temperatures. High hydrostatic pressure, ultrasonication, and pulsed electric fields were the most discussed non-thermal technologies. At the same time, ohmic heating and microwave heating were the most reported thermal technologies. Furthermore, the most used applications, critical process parameters, and food properties to be evaluated are highlighted and discussed. The results could be used as a basis for the dairy processors to implement non-conventional technologies as an option at their production lines, as they demonstrate the most relevant process parameters and food characteristics to be evaluated, helping them to choose the parameters with higher impact and firstly consider them. Furthermore, consumers studies are important and should evaluate consumer perception about the products and the perceived benefits and risks of the novel technologies.     

Alternatives to conventional thermal treatments in fruit-juice processing. Part 1: Techniques and applications

This paper provides an overview of alternatives to conventional thermal treatments and a review of the literature on fruit-juice processing for three key operations in fruit-juice production such as microbial inactivation, enzyme inactivation, and juice yield enhancement, these being radiation treatments (UV light, high-intensity light pulses, γ-irradiation), electrical treatments (pulsed electric fields, radiofrequency electric fields, ohmic heating), microwave heating, ultrasound, high hydrostatic pressure, inert gas treatments (supercritical carbon dioxide, ozonation), and flash-vacuum expansion. The nonthermal technologies discussed in this review have the potential to meet industry and consumer expectations. However, the lack of standardization in operating conditions hampers comparisons among different studies, and consequently ambiguity arises within the literature. For the juice industry to advance, more detailed studies are needed on the scaling-up, process design, and optimization, as well as on the effect of such technologies on juice quality of juices in order to maximize their potential as alternative nonthermal technologies in fruit-juice processing.     

Validation of process technologies for enhancing the safety of low-moisture foods: A review

The outbreaks linked to foodborne illnesses in low-moisture foods are frequently reported due to the occurrence of pathogenic microorganisms such as Salmonella Spp. Bacillus cereus, Clostridium spp., Cronobacter sakazakii, Escherichia coli, and Staphylococcus aureus. The ability of the pathogens to withstand the dry conditions and to develop resistance to heat is regarded as the major concern for the food industry dealing with low-moisture foods. In this regard, the present review is aimed to discuss the importance and the use of novel thermal and nonthermal technologies such as radiofrequency, steam pasteurization, plasma, and gaseous technologies for decontamination of foodborne pathogens in low-moisture foods and their microbial inactivation mechanisms. The review also summarizes the various sources of contamination and the factors influencing the survival and thermal resistance of pathogenic microorganisms in low-moisture foods. The literature survey indicated that the nonthermal techniques such as CO₂, high-pressure processing, and so on, may not offer effective microbial inactivation in low-moisture foods due to their insufficient moisture content. On the other hand, gases can penetrate deep inside the commodities and pores due to their higher diffusion properties and are regarded to have an advantage over thermal and other nonthermal processes. Further research is required to evaluate newer intervention strategies and combination treatments to enhance the microbial inactivation in low-moisture foods without significantly altering their organoleptic and nutritional quality.     

Effects of high‐pressure processing on fungi spores: Factors affecting spore germination and inactivation and impact on ultrastructure

Food contamination with heat‐resistant fungi (HRF), and their spores, is a major issue among fruit processors, being frequently found in fruit juices and concentrates, among other products, leading to considerable economic losses and food safety issues. Several strategies were developed to minimize the contamination with HRF, with improvements from harvesting to the final product, including sanitizers and new processing techniques. Considering consumers’ demands for minimally processed, fresh‐like food products, nonthermal food‐processing technologies, such as high‐pressure processing (HPP), among others, are emerging as alternatives to the conventional thermal processing techniques. As no heat is applied to foods, vitamins, proteins, aromas, and taste are better kept when compared to thermal processes. Nevertheless, HPP is only able to destroy pathogenic and spoilage vegetative microorganisms to levels of pertinence for food safety, while bacterial spores remain. Regarding HRF spores (both ascospores and conidiospores), these seem to be more pressure‐sensible than bacterial spores, despite a few cases, such as the ascospores of Byssochlamys spp., Neosartorya spp., and Talaromyces spp. that are resistant to high pressures and high temperatures, requiring the combination of both variables to be inactivated. This review aims to cover the literature available concerning the effects of HPP at room‐like temperatures, and its combination with high temperatures, and high‐pressure cycling, to inactivate fungi spores, including the main factors affecting spores’ resistance to high‐pressure, such as pH, water activity, nutritional composition of the food matrix and ascospore age, as well as the changes in the spore ultrastructure, and the parameters to consider regarding their inactivation by HPP.     

Combining nonthermal technologies to control foodborne microorganisms

Novel nonthermal processes, such as high hydrostatic pressure (HHP), pulsed electric fields (PEFs), ionizing radiation and ultrasonication, are able to inactivate microorganisms at ambient or sublethal temperatures. Many of these processes require very high treatment intensities, however, to achieve adequate microbial destruction in low-acid foods. Combining nonthermal processes with conventional preservation methods enhances their antimicrobial effect so that lower process intensities can be used. Combining two or more nonthermal processes can also enhance microbial inactivation and allow the use of lower individual treatment intensities. For conventional preservation treatments, optimal microbial control is achieved through the hurdle concept, with synergistic effects resulting from different components of the microbial cell being targeted simultaneously. The mechanisms of inactivation by nonthermal processes are still unclear; thus, the bases of synergistic combinations remain speculative. This paper reviews literature on the antimicrobial efficiencies of nonthermal processes combined with conventional and novel nonthermal technologies. Where possible, the proposed mechanisms of synergy is mentioned.