Introduction

The current demand for safer, healthier, and more nutritious food products has boosted the search for new manufacturing strategies. Conventional thermal treatments, such as pasteurization (60 to 100 °C) and sterilization (up to 140 °C), have been applied to produce safe food products. Heat treatments ensure consumer safety through the inactivation of pathogenic and spoilage microorganisms and endogenous enzymes of foods and beverages (Ağçam et al., 2018; Lima Gomes et al., 2020; Muñoz et al., 2018). However, severe thermal treatments can cause undesirable changes in sensory attributes of food products. Likewise, nutrients also are affected after heat processing. Degradation of vitamins and thermolabile bioactive compounds and protein denaturation can be verified in thermally treated products. Therefore, there is a growing demand for non-thermal technologies or those that use a lower process temperature to inactivate microorganisms and enzymes in foods and beverages. These innovative technologies are also evaluated to minimize product degradation, maintaining the aspects and characteristics of the fresh or unprocessed product (Chen et al., 2010; Monteiro et al., 2018).

New processes based on low-frequency (16 to 100 kHz) and high-power (> 1 W/cm2) ultrasound technology have been proposed as a potential alternative to conventional heat treatments. In this way, limitations and drawbacks concerning the application of severe heat processing in food products have been overcome using acoustic energy. Additionally, this technology has been recognized for enabling clean or green processes. Ultrasound-assisted processes for phytochemical extraction (Sukor et al., 2021; Tekin et al., 2015), food stabilization (Saeeduddin et al., 2015; Yildiz et al., 2020), emulsification (Huerta et al., 2020; Silva et al., 2015), and chemical modification of macromolecules (Chen et al., 2019; Zhong & Xiong, 2020) promote less impact on natural resources than conventional processes. Ultrasound technology enables the reduction or even elimination of the use of toxic solvents, besides shorter processing times, and consequently less energy expenditure and operational cost. Therefore, ultrasound technology is promising for developing new sustainable food production systems (Guimarães et al., 2019; Oladunjoye et al., 2021; Scudino et al., 2020; Tappi et al., 2020).

Innovative food stabilization processes based only on the application of acoustic energy have been assessed for different products (Ansari et al., 2017; Inmanee et al., 2020; Križanović et al., 2020; Režek Jambrak et al., 2017). Despite that, studies concerning the synergistic effect of acoustic cavitation combined with mild thermal treatments (~ 50 to 70 °C) have increased in the last years. Combined treatments can enhance the inactivation of microorganisms and enzymes in foods without compromising their sensory and nutritional quality. The combination of acoustic energy and mild heat treatment is known as thermosonication (Bansal et al., 2018). The beneficial effects of thermosonication processing have been observed on vegetables (Cruz et al., 2007; Mansur & Oh, 2015), fruit and vegetable juices (Anaya-Esparza et al., 2017a, b; Jabbar et al., 2015), meat products (Inmanee et al., 2020; Pennisi et al., 2020), dairy products (Gursoy et al., 2016; Ragab et al., 2019), fermented beverages (Deng et al., 2018; Milani & Silva, 2017), and others (Al-Juboori et al., 2012; Zhong & Xiong, 2020).

In this context, this review evaluate the impact of thermosonication processing on the safety and quality aspects of different foods and beverages. The challenges and advantages of this emerging technology were discussed in contrast to conventional heat treatments. Also, the process design of ultrasound combined with mild thermal treatments was assessed.

Fundamentals of Ultrasound Technology

Sound is a mechanical wave that propagates longitudinally, promoting compression and rarefaction of atmospheric air throughout its propagation due to instantaneous pressure variations. The sound can be classified as infrasound (≤ 20 Hz) and ultrasound (≥ 20 kHz) (Alves et al., 2013; Cárcel et al., 2012; Yu et al., 2020). The frequency range of the ultrasound also defines its technological application since ultrasound technology is divided into processes based on low frequency (20 a 100 kHz) and high frequency (> 100 kHz) (Kentish & Feng, 2014; Knorr et al., 2004).

Figure 1 presents the applicability of ultrasound technology according to the intensity and frequency of energy provided by the ultrasonic system. Low-energy and high-frequency ultrasound technology is applied for imaging diagnostic analysis (Correia et al., 2008; Elvira et al., 2005). In contrast, high-energy and low-frequency ultrasound waves are applied in liquid systems to promote mechanical, physical, and chemical changes (Monteiro et al., 2020; Strieder et al., 2020).

Fig. 1
figure 1

Classification of the ultrasound applicability according to the energy intensity and frequency supplied by the ultrasonic system

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Acoustic energy has been characterized in the literature in different ways (Knorr et al., 2004):

  • Acoustic power: refers to the amount of energy delivered by the ultrasonic system to each unit of time (energy/time)

  • Acoustic power intensity: the ratio between acoustic power emitted by the ultrasonic system and the emission area (power/area)

  • Acoustic power density: the ratio between acoustic power emitted by the ultrasonic system and the volume of the sonicated medium (power/volume)

Since most sonication processes were carried out on a laboratory scale, the magnitudes of intensity and density are commonly presented in the units of W/cm2 and W/cm3, respectively. The acoustic energy provided by the ultrasonic system also can be expressed considering the processing time. Equation 1 presents the energy density that expresses the energy applied per volume. Equation 2 shows the specific energy that expresses the energy delivered per mass (Strieder et al., 2020).

$$Energy\ density\left[\frac{Energy}{Volume}\right]=\frac{Ultrasound\ power\times Processing\ time}{Volume}$$
(1)
$$Specific\ energy \left[\frac{Energy}{Mass}\right]=\frac{Ultrasound\ power\times Processing\ time}{Mass}$$
(2)

Acoustic cavitation is a physical phenomenon that occurs due to the application of low-frequency and high power ultrasound in liquid media. Ultrasound waves promote alternative cycles of compression and rarefaction (expansion) of the molecules of a liquid medium (Swamy et al., 2020). This leads to pressure fluctuations in the liquid medium that favor the formation of bubbles throughout the expansion cycle. The bubble formation starts when a high negative pressure exceeds the tensile strength of the liquid. The produced bubbles absorb small amounts of vapor from the liquid and continue to grow. The bubbles explode, releasing energy when they reach a critical size (Yu et al., 2020). This energy is transformed or released in various forms (microjet, heat, or chemical reactions) throughout the bubble collapse stage (Wu et al., 2020). Thus, acoustic cavitation this phenomenon performs the main effect of the ultrasound application in food matrices (Marques Silva & Sulaiman, 2017).

The cavitation intensity depends on the energy converted to acoustic cavitation during sonication (Soltani-Firouz et al., 2019). Frequency influences the bubble size and, consequently, also impacts the cavitation intensity. Low-frequency ultrasound generates transient cavitation, characterized by the formation of large unstable bubbles that can collapse violently. The violent collapse generates points of high temperature and pressure in the sonicated medium (Soltani-Firouz et al., 2019; Welti-Chanes et al., 2017). Different ultrasonic frequencies from the same acoustic intensity provide different acoustic pressures and wave interactions in the liquid medium. The higher the ultrasonic frequencies (> 80 kHz), the shorter the period and, consequently, the shorter the wavelength. Thus, bubbles produced will not have enough time to execute the collapse mechanism (Rashwan et al., 2020).

In addition to frequency, the physical properties of the sonicated medium, such as viscosity, density, surface tension, and vapor pressure, also affect acoustic cavitation. Tzanakis et al. (2017) demonstrated that the impact of vapor pressure, surface tension, and viscosity, plays a decisive role in the development and activity of cavitation in sonicated liquids. A high viscosity contributed to the cushioning of bubble oscillations in glycerin. Thereby less violent collapses were observed with energy dissipation into the medium. High energy amplitudes are required for greater penetration of acoustic radiation into high viscosity liquids due to their greater resistance to acoustic energy (O’Sullivan et al., 2018). On the other hand, liquids with low vapor pressure generate fewer cavitation bubbles and, consequently, less bubble collapse. Thus, there is less conversion of acoustic energy into heat in the sonicated medium (Merouani et al., 2018).

Acoustic energy can also cause different effects on the sonicated matrices depending on the frequency, power, processing time, amplitude, and temperature conditions. The explosion of the cavitation bubbles explosion generates microjets that promote shear forces on products, specifically on the external surface of cellular tissues (plant or animal), the cell wall of microorganisms, and on particles, such as starch granules and sugar crystals. The formation of cracks and pores in the physical structures induced by low-frequency and high-power ultrasound is known as sonoporation (Knorr et al., 2004; Yu et al., 2020). The sonoporation is responsible for microbial inactivation and extraction of phytochemicals because it promotes cell lysis of microorganisms and disruption of plant cell structures (Guo et al., 2020; Tabib et al., 2020). In addition to sonoporation, acoustic cavitation may favor the production of reactive species and free radicals. The decomposition of the water molecule under sonication can generate free radicals, such as H+ and OH−. These can also recombine to form hydrogen peroxide (H2O2). The chemical changes in the liquid medium attributed to acoustic cavitation contribute to microbial inactivation. Free radicals, together with localized heating, can lead to the thinning of the microbial cell membrane. Microbicidal properties of hydrogen peroxide also act synergistically for microbial inactivation (Dolas et al., 2019; Swamy et al., 2020). Free radicals can also react with the amino acids of enzymes affecting their activity and catalytic function (Marques Silva & Sulaiman, 2017).

The characteristics and properties of the matrices, such as their physical properties and composition, also impact the sonoporation results. Recent reviews have demonstrated new proposals for the application of ultrasound technology, such as for the growth of beneficial microorganisms in probiotic cultures (Guimarães et al., 2019), improvements in the functional properties of polymers (Wang et al., 2020), and a promising alternative for producing food flavors obtained from the Maillard reaction (Yu et al., 2020).

Ultrasound System

Figure 2 presents ultrasonic systems. They are composed of an electric power generator, a transducer, and an emitter, which produce ultrasonic waves in the liquid medium. The two configurations most used are probe-type ultrasound, in which a probe is used as an emitter, and bath-type ultrasound (Fig. 2) (Bermúdez-Aguirre et al., 2011; Welti-Chanes et al., 2017). The application of acoustic energy in food products can be carried out directly or indirectly (Miano et al., 2017; Rashwan et al., 2020). However, energy is usually applied directly to the sample using probe-type ultrasound (Miano et al., 2017). In this application, food matrices are placed in a container, and the ultrasonic probe is subsequently immersed inside it (Fig. 2). Figure 2 presents an example using the bath system. The matrices are placed inside a container that is inside the bath. The bath stays filled with liquid that can be water. Thus, acoustic energy is supplied to matrices at the bottom of the ultrasonic bath, where the transducers are located. Probe ultrasonic systems provide high acoustic intensity (W/cm2) into a liquid system confined in the vessel or chamber. In contrast, ultrasonic bath systems allow a greater liquid volume in the chamber, and their transducers have a large surface area. In this way, they can provide a low acoustic intensity and low acoustic power density compared to ultrasonic probes (Kentish & Feng, 2014). Therefore, the energy intensity required in the processing defines the condition and type of ultrasonic system to be used (Kentish & Feng, 2014).

Fig. 2
figure 2

Ultrasound equipment and types of ultrasonic systems

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The probe diameter is an important characteristic of the ultrasound system (Bermúdez-Aguirre et al., 2011). O’Sullivan et al. (2018) observed that a 3-mm diameter probe generated higher acoustic intensity in a liquid medium than a 12-mm probe. A smaller probe diameter provided greater penetration and, thus, a better distribution of acoustic cavitation. The probe shape also affects the acoustic energy transmission and, consequently, the cavitation efficiency. Conical probes generate a larger cavitation zone by increasing the amplitude of the waves and thus improving the process efficiency (Fang et al., 2018). The acoustic cavitation performance also depends on the geometry and ultrasound reactor size because they impact acoustic pressure. For the application of acoustic energy directly on scales larger than the laboratory, higher ultrasonic amplitudes would be needed to achieve a larger area and greater cavitation intensity (Rashwan et al., 2020).

Thermosonication

Thermosonication is a technique that combines the application of acoustic energy with mild moderate heat treatments. Therefore, the acoustic energy and the heat act simultaneously on the cell structures, promoting the inactivation of pathogenic and spoilage microorganisms and endogenous enzymes (Amador-Espejo et al., 2020). Thermosonication treatments are energetically more efficient because they promote microbial and enzymatic inactivation in shorter holding times (Sango et al., 2014; Welti-Chanes et al., 2017). According to the temperature range employed, the process can be classified as sub-lethal (< 45 °C) and lethal (> 45 °C) (Anaya-Esparza et al., 2017a, b).

The temperature control during thermosonication processing is critical to ensure its effectiveness. Since high temperatures can affect nutritional and sensory properties altering food quality. Furthermore, high temperatures can attenuate the action of acoustic cavitation in liquid media. The temperature rise promotes an increase in the vapor of pressure of liquids decreasing their viscosity. In its turn, lower viscosities favor the cavitation bubbles formation. However, the bubbles formed in this low-viscosity liquid medium contain more steam, which reduces their collapse intensity. Thus, the energy released throughout bubble eclosion is reduced. This phenomenon is known as the damping effect (Sango et al., 2014; Ugarte-Romero et al., 2007). Therefore, there is an optimum temperature to be reached for each ultrasound process for obtaining the best acoustic cavitation performance and the desired effects (Schössler et al., 2014).

In this regard, the heat provided by an external source during the thermosonication treatment is an additional energy since sonication treatment alone promotes a temperature rise in the liquid medium. On the other hand, in some processes, the increase temperature provided by sonication is undesirable. Thus, cooling circulating baths are widely employed to reduce the temperature increase. Another alternative is setting up the ultrasound equipment to apply pulses of energy. For example. using 5 s on/10 s off or 5 s on/5 s off, as opposed to a continuous power supply (Marques Silva & Sulaiman, 2017). In thermosonication processing, heating circulating baths are used to provide thermal energy and maintain the working temperature throughout the treatment. However, in most cases, the working temperature conditioned by the external heat source is not the actual temperature of the thermosonication treatment because sonication also provides thermal energy to the sonicatedmedium due to acoustic cavitation. For example, thermosonication processes carried out at mild temperatures between 40 and 70 °C can reach high process temperatures, such as 100 °C, depending on applied acoustic energy conditions, such as ultrasound intensity and power density Therefore, temperature monitoring throughout thermosonication processing is fundamental to ensure the maintenance of nutritional and sensory quality aspects of thermosonicated food products.

Thermosonication on Food Processing

Plant Products

Plant products, such as fruit and vegetable juices and fresh fruits and vegetables, were grouped in this section. Table 1 presents the main remarks regarding thermosonication processing on this plant-based products. Thermosonication treatments have been evidenced as a promising technique for the inactivation of microorganisms and enzymes of plant products. Fruit and vegetable juices have been subjected to a shorter exposure time to high temperatures during thermosonication treaetment. Thus, this emerging technology has allowed the maintenance or even increased availability and retention of bioactive compounds in products, including throughout their storage.

Table 1 Thermosonication effects on the safety and quality aspects of plant products
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After the thermosonication treatment (45 kHz, 40 °C, 30 min) of a whole tomato sample, Pinheiro et al. (2019) observed an 8% reduction in the total phenolic compounds content. However, they verified an increase of 26% after 15 days of storage. This effect was attributed to the sonoporation of cell structures, which potentiated the bioaccessibility of phenolic compounds. A reduction in the total phenolic content was also observed in thermosonicated red pitaya juice samples. The working temperature had a significant impact on the degradation of phenolic compounds. The higher working temperature of 50 °C (475 W, 20 min) also reduced the retention of bioactive compounds (Liao et al., 2020). Similar behavior was observed for thermosonicated carrot juice samples (20 kHz, 48 W/cm2, 10 min) according to Jabbar et al. (2015). A significant reduction in the total phenolic compounds, flavonoids, tannins, and ascorbic acid content was associated with the working temperature rise from 40 to 60 °C. Despite this, the retention levels of bioactive compounds in thermosonicated juices were higher than in thermally treated juices at 80 °C for 1 min. On the other hand, all thermosonicated juice samples presented higher total carotenoid content than fresh juice and heat-treated. The disruption of cell membranes and protein-carotenoid complex contributed to the carotenoids extraction throughout thermosonication treatment (Jabbar et al., 2015). Different results were observed in thermosonicated hazelnut-based non-dairy alternative milk (Atalar et al., 2019). Thermosonication treatments (20 kHz, 750 W, 40–80% amplitude) promoted a significant increase in the phenolic compound contents of the samples. The treatment applying 60% amplitude for 20 min increased the phenolic content from 162.78 to 178.82 µg GAE/g, which increased the antioxidant activity. Atalar et al. (2019) attributed these results to the sonoporation of the cell walls. The sonoporation contributed to the disruption of cell structures, favoring the release of bioactive phytochemical compounds.

Thermosonication did not promote significant changes in pH, acidity index, and total solids content of hazelnut-based non-dairy alternative milk (Atalar et al., 2019), carrot juice (Jabbar et al., 2015), fruit smoothie (Amador-Espejo et al., 2020), soursop puree (Martínez-Moreno et al., 2020), and pumpkin juice (Demir & Kılınç, 2019). On the other hand, different effects on the color attributes were observed after thermosonication treatments. The reconstituted orange juice samples presented smaller changes (ΔE = 1.8) in their color instrumental parameters after thermosonication processing (30 kHz, 500 W, 55 °C, 10 min) compared to heat treatment at 94 °C for 26 s (ΔE = 2.7) (Walkling-Ribeiro et al., 2009). However, fresh orange juice samples thermosonicated at 20 kHz and 47 °C applying a nominal power of 300 W for 30 min presented changes in their color parameters ΔE > 3.0 (Wahia et al., 2020). Longer processing times (> 20 min) and temperatures above 50 °C also led to a visual color change (ΔE > 3.0) in red pitaya juice. Despite that, no difference concerning visual color appearance was observed between thermosonicated and untreated pitaya juice samples. Also, UV–visible absorbance spectra demonstrated that thermosonication processes were more efficient in preserving the color of the juice than heat treatment at 83 °C for 1.5 min (Liao et al., 2020). Thermosonication treatment also delayed the development and ripening of the color of tomatoes. The ultrasound processing combined with mild heat treatment possibly inhibited the ethylene production in tomatoes and delayed other ripening processes. Color changes in fruit and aroma development were associated with acoustic cavitation, which may have promoted an adverse effect on the tomato’s pigment stability (Pinheiro et al., 2016, 2019). Therefore, thermosonication processing can cause different impacts on the plant products’ color depending on process conditions and the characteristics of the product.

Meat Products

Studies related to thermosonication of meat products, such as fish, sausage, chicken, and beef, were grouped in this section. Thermosonication treatments have been less efficient in microbial inactivation of these products, mainly of meat. The chemical and physicochemical nature of the meat is the primary reason for this low efficiency. Meat and meat products present nutrients and a pH range that can benefit the development, adhesion, or even the protection of microorganisms. Besides that, studies have been observed that aerobic bacteria are more resistant to thermosonication treatments. The formed set of gram-negative and gram-positive bacteria on the skin of the chicken difficult their inactivation. Gram-positive bacteria have thicker cell walls that physically protect other microorganisms making them more resistant to thermosonication. In this way, another practical and promising strategy is the combination of thermosonication with other treatments for industrial applications. These other treatments have been employed in chemical products or thermal shocks to enhance the microbial inactivation of meat products. Table 2 presents some examples of thermosonication effects on meat products.

Table 2 Thermosonication effects on the safety and quality aspects of meat products
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Inmanee et al. (2020) evaluated the thermosonication treatment of pork sausage at 80 °C and 40 kHz applying a nominal power of 150 W. They observed that the innovative treatment did not affect the sensory characteristics and the chemical properties of the product. However, longer processing times (> 20 min) affected more the texture characteristics, such as the hardness, elasticity, cohesiveness, and chewability, of the sausages than conventional pasteurization at 80 °C for 15 min. The best thermosonication condition for sausages processing was 80 °C for 20 min. This process condition inactivated total bacteria, molds, and yeast in the sausages. After 30 days of cold storage at 4 °C, the sausages presented a small microbiological load of 5.0 × 101 CFU/g and less than 1 log CFU/g for total bacteria and molds and yeasts, respectively. Additionally, the thermosonication treatment promoted the extension of the self life of the sausages, maintaining their quality attributes.

Kassem et al. (2018) observed that the increase in working temperature and processing time caused a higher decrease in the microbial load of the thighs of raw chickens after thermosonication processing. The thermosonication treatment at 54 °C for 3 min applying 80 W/L as an individual treatment promoted a low inactivation of Campylobacter jejuni and total enterobacteriaceae. Also, this process condition did not affect total viable count (TVC). However, the combination of thermosonication processing with chemical treatments enhanced the microbial load reduction. The combination of sodium decanoate (3%) + thermosonication (54 °C, 3 min, 80 W/L) enhanced the inactivation of the microbial load. Similar results were reported by Haughton et al. (2012). They observed higher resistance of TVCs to thermosonication treatments using energy densities of 20 kW/L and 20 W/L at 53 °C for 16 min. However, C. jejuni and enterobacteriaceae groups were more sensitive to thermosonication treatments. The count of these microorganisms was reduced to undetectable values using an energy density of 20 kW/L. The resistance of the aerobic bacteria was associated with the variety of microorganisms present in the chicken’s skin. Gram-positive bacteria and spore-forming bacteria may be more resistant to sonication than gram-negative bacteria.

Evelyn and Silva (2015b) observed a low inactivation of two strains of Clostridium perfringens spores (NZRM 2621 and NZRM 898) in a beef paste. A slight logarithmic reduction of 1 and 1.5 was observed after 60 min of thermosonication at 75 °C and 24 kHz, applying 33 W with a specific energy of 0.33 W/g. An association of treatments was proposed to enhance the inactivation microorganism. The authors combined a thermal shock treatment at 80 °C for 10 min with thermosonication at 24 kHz applying 162 W and energy density of 16.2 W/mL using different temperatures (75 to 105 °C). The combination of thermal shock + thermosonication treatment doubled spore inactivation. However, temperatures higher than 85 °C were required to ensure C. perfringens spores inactivation.

Pennisi et al. (2020) evaluated the effect of thermosonication treatments on the inactivation Listeria monocytogenes inactivation in smoked salmon. Thermosonication treatments (800 W, 20 kHz) at 30 and 40 °C for 15 min and 50 °C for 5 min promoted the same microbial load reduction of 2.19 log CFU/g. The processes carried out at 40 and 50 °C for 10 min also promote low inactivation of L. monocytogenes. The resistance of L. monocytogenes to thermosonication may be associated with the damping effect of the matrix. Also, thermosonication treatments did not modify the sensory characteristics of the salmon samples, such as flavor and color.

Dairy Products

Thermosonication treatments have been applied to milk and dairy products to inactivate their microbial load. Additionally, products prepared with thermosonicated milk have shown different characteristics of water retention, viscosity, consistency, syneresis, and sedimentation. Thermosonication processing has promoted the kinetic stability of the dairy productss by the reduction in the droplet size distribution of milk emulsions. The self size dairy products also has been extended by the inactivation of pathogenic microorganisms naturally found in milk. Table 3 presents the main remarks of these thermosonication effects on milk and dairy products.

Table 3 Thermosonication effects on the safety and quality aspects of dairy products
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Erkaya et al. (2015) applied thermosonication treatments on the milk to improve the technological properties of Ayran, an acidified milk beverage. The sample produced with thermosonicated milk presented an increase in water retention capacity and viscosity. The thermosonicated sample at 70 °C for 3 min presented 31% less of the syneresis/phase separation than the control sample. This effect was still observed in the samples for up to 30 days after their processing. The increase of ultrasonic power (100 to 150 W) also reduced the phase separation (21 to 0%) of the acidified milk. minThe yogurt produced with thermosonicated milk (70 °C for 15 min) also presented a higher apparent viscosity than the control sample (Gursoy et al., 2016). These effects were observed up to 10 days after processing. According to the authors, thermosonication treatment promoted the dissociation of the casein micelles in subunits, which favored the formation of strong networks by aggregating the subunits between them and/or partially denatured whey proteins throughout the fermentation step. These strong networks improved the gel structure formation in the yogurt samples produced with thermosonicated milk. Another study carried out by Riener et al. (2010) demonstrated that the thermosonicated milk samples produced stronger yogurt gels, even with a low-fat content (0.1%). However, the firmness of the yogurt gels produced with thermosonicated milk (10 min at 400 W) was not associated with a whey protein denaturation. The percentage of whey protein denaturation was 26.0, 26.9, and 28.1%, for skimmed (0.1%), semi-skimmed (1.5%), and whole milk (3.5%), respectively. In contrast, the milk samples treated by a conventional thermal process at 90 °C for 10 min presented 49.1, 49.3, and 52.2% of whey protein denaturation for the skimmed, semi-skimmed, and whole milk, respectively (Riener et al., 2009).

Almanza-Rubio et al. (2016) also evaluated the use of thermosonicated milk to manufacture cream cheese. They attributed the cheese water retention (from 55 to 60%) and production yield (from 10.9 to 19.5%) to the synergistic effect between acoustic energy and heat treatment. The denatured whey proteins showed greater binding capacity with the casein micelles. Thermosonication processing also promoted the formation of large aggregates with casein micelles and reduced the milk fat globules diameter from 7 μm to values below 2 μm. This size reduction improved cheese fat retention. The authors also observed an increase in the interactions between fat globules and fat globules-proteins, possibly due to an alteration in the fat globule membrane. The cream cheese produced with thermosonicated milk also presented better texture and rheological properties, besides thermal stability (Almanza-Rubio et al., 2016).

Fermented Beverages

Few studies have evaluated the thermosonication effects on wine and beer production. Additionally, most of these studies examined the impacts of thermosonication processing on the inactivation of microorganisms, such as Brettanomyce bruxellensis, Saccharomyces cerevisiae, and Lactobacillus acetotolerans, responsible for the deterioration of these drinks. Thermosonication treatments have induced the transformation of these microorganisms to a viable putative non‐culturable (VPNC) state. The beverages’ alcohol content and pH of the beverages have not influenced the thermosonication effects on microbial inactivation. However, the sugar content of the beverage can help in the adaptation of microorganisms to adverse conditions promoted by thermosonication treatment. Furthermore, thermosonication did not affect the sensory attributes and physicochemical properties of fermented drinks. Table 4 presents the studies concerning the impact of thermosonication processing on the safety and quality aspects of beer and wine.

Table 4 Thermosonication effects on the safety and quality aspects of fermented beverages
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Deng et al. (2018) evaluated thermosonication treatments (538.7 W and 24 kHz) at 50 and 60 °C for 2 min on microbial inactivation of lager beer. These treatments inactivated yeast, lactic acid bacteria, and mesophilic microorganisms similarly to the conventional heat pasteurization at 60 °C for 15 min. Beer quality parameters, such as pH, ethanol content, and bitterness, were not affected after thermosonication processing. Furthermore, the foam stability of the thermosonicated beer samples was enhanced. Likewise, beer samples subjected to thermosonication processing at 50 °C had long-term stability concerning their color, flavor, and oxidative stability. Other studies have also evaluated the inactivation of L. acetotolerans CGMCC 7.150 in larger beers through thermosonication processing (Piao et al., 2019; Yin et al., 2018). Piao et al. (2019) observed that low power densities (0.6, 1.2, or 1.8 W/mL, 24 kHz) induced the transformation of the L. acetotolerans cells to VPNC state. However, the application of 2.4 W/mL for 12 min at 24 kHz resulted in a beer with a lower viable cell count (almost zero). In this way, thermosonication can inactivate exponentially growing and VPNC cells. Yin et al. (2018) also observed that the cells of L. acetotolerans in the VPNC state are more resistant to thermosonication treatments than cells in the normal state. They applied 8.9 W/mL at 24 kHz and 40 °C for 4 min and observed a reduction of normal cells in 6 log cycles. An energy density of 8.9 W/mL at 60 °C and 24 kHz was required to inactivate the same amount of VPNC cells.

Different alcohol contents (0.0, 4.8, and 7.0% v/v ethanol) promoted the same effects on the Saccharomyces cerevisiae ascospores inactivation in beer samples subjected to thermosonication processing. However, process parameters, such as holding time and temperature, affected the ascospores inactivation. A logarithmic reduction of 3.6 log cycles was achieved by applying 16.2 W/mL at 24 kHz for 20 min. Additionally, the batch processing resulted in a higher inactivation of the microbial load compared to the continuous process. The differences between the results achieved in each type of process were related to specific energies applied. In the continuous process, lower energy density (10.8 W/mL) was applied to the beer samples compared to the batch process (16.2 W/mL) for the same holding time (Milani & Silva, 2017). Therefore, higher specific densities favored the inactivation of S. cerevisiae ascospores.

Otherwise, Križanović et al. (2020) reported that the sugar content of the red wine and thermosonication holding time significantly influenced the reduction in the cultivability of Brettanomyces bruxellensis CBS 2499. Higher sugar content ensured yeast adaptation to unfavorable conditions promoting a protective effect. In contrast, longer holding times were associated with a total reduction in the yeast cultivability. Thermosonication processing also induced the yeast to pass for a VPNC state in dry wines (without sugar) after 3 min of treatment applying 600 W at 43 °C and 20 kHz, which affected 20.5% of yeast viability. The yeast’s metabolic activity also was affected by thermosonication after 90 days of storage. Lower production of deteriorating compounds was observed in wines with a higher ethanol content (14%) and lower pH values (3.5 and 3.7) after storage time. However, the sugar content promoted the growth and proliferation of yeast in the wine, increasing the production of deteriorating compounds (4-ethylphenol and 4-ethylguaiacol). Lyu et al. (2016) studied the impacts of thermosonication on Chinese rice wine. The higher S. cerevisiae inactivation (< 1.2 log CFU/mL) was achieved by applying higher nominal power and a low working temperature (750 W at 40 °C and 20 kHz) for 60 min. The low S. cerevisiae inactivation may be due to the high carbohydrate content of rice. As explained earlier, carbohydrates can protect the yeast against thermosonication treatment. Additionally, a lower power density of 5 W/mL was applied in this study compared to the power density of 16.2 W/mL used to inactivate ascospores in beers, as mentioned earlier.

Impact of the Food Matrix on Thermosonication Efficiency

Some intrinsic characteristics of each food group hinder the microbial or enzyme inactivation through thermosonication. On the other hand, the combined effect of acoustic energy and mild heat treatments can modify food the physicochemical and technological properties of the food products. In this topic, the characteristics of each food product (plant, meat, dairy, and fermented beverage) were grouped to emphasize those most affected the thermosonication efficiency.

Plant Products

The main objective of the application of thermosonication on plant products, such as fruit and vegetables and their juices and beverages, has been the inactivation of microorganisms and enzymes. Thus, many studies aimed to reduce the microbial load and enzyme activity, avoiding bioactive compounds degradation. Several studies reported losses in these compounds using high thermosonication temperatures and holding times. Thus, the thermal resistance of bioactive phytochemical compounds is the most relevant characteristic of plant products. Thermosonication treatments must be performed to inactivate microorganisms and enzymes at temperatures that preserve these phytochemical.

Meat Products

Thermosonication treatments have been applied to meat products for microbial inactivation. However, some strains of microorganisms, such as gram-positive bacteria, are resistent to these treatments. Thus, the identification of the microorganisms present in each meat product is a crucial factor to be considered in the processing of this food group. Thereby, thermosonication can be applied to inactivate these resistant microorganisms combined with natural chemical agents.

Dairy Products

Thermosonication treatments have been applied to milk to inactivate microorganisms and improve the technological properties of their derivatives. The microbial inactivation of dairy products through ultrasound processing is describe in the literature (Guimarães et al., 2018; Scudino et al., 2020). High acoustic energy is required for the inactivation of microorganisms in milk. On the other hand, the impact of thermosonication on the technological properties of dairy products has been discussed in the literature recently. The application of thermosonication in these products has mainly promoted the breakdown of fat globules and structural changes in dairy proteins. In this way, technological characteristics associated with texture and rheological properties, such as water retention, viscosity, consistency, spreadability, viscoelastic, and kinetic stability, have been affected. Therefore, different thermosonication process conditions can affect the fats and proteins of dairy products, promoting several technological changes.

Fermented Beverage

Few studies were carried out, but they reported that the wine sugar content difficult the thermosonication action on the inactivation of enzymes. Sugar promotes a protective effect on wine yeast. Therefore, the sugar content must be considered in thermosonication treatments focused in microbial and enzymatic inactivation.

Impact of Thermosonication Processing on the Microbial Inactivation

Most thermosonication treatments have been performed for the microbial inactivation of food products. Ramteke et al. (2020) and Anaya-Esparza et al. (2017a, b) reviewed more specifically the effects of thermosonication on the microbial inactivation of dairy and plant products, respectively. They explain some theories about the possible mechanisms for the inactivation of microorganisms during thermosonication. Most agree that the acoustic cavitation is the main effect responsible for microbial inactivation. In addition to thermal effects, acoustic cavitation weakens the cell membrane of microorganisms due to shear stress (Bermudez-Aguirre et al., 2011). This cell membrane weakening and/or rupture promote the leakage of the internal content of the cellular organelles. Thus, a lethal or sub-lethal effect on microbial cells and spores is observed (Anaya-Esparza et al., 2017a, b; Bermudez-Aguirre et al., 2011; Wordon et al., 2012). In this section, we discussed the impact of thermosonication on the activation of microbial suspensions. Table 5 presents some examples of these impacts on the inactivation of microbial suspensions usually associated with technological issues of food products.

Table 5 Impact of the thermosonication treatment on the inactivation of microbial suspensions
Full size table

Fan et al. (2019a, b) demonstrated that thermosonication causes damage to the internal membrane of Bacillus subtilis spores favoring their inactivation. Despite thermosonication ability to promote microbial inactivation, the effectiveness of this treatment is strongly affected by the morphology (shape or size) and the intrinsic characteristics of microorganisms. Some of these are more resistant to adverse conditions. Deshpande and Walsh (2020) obtained smaller reductions in the spore count of B. subtilis compared to vegetative cells of Geobacillus stearothermophilus and Anoxybacillus flavithermus applying the same holding times. In another study, only 1.8 log cycles of Byssochlamys nivea spores were inactivated at 75 °C and 24 kHz applying 0.33 W/mL for 15 min. However, thermosonication processing carried out for 30 min demonstrated the same or higher viable spore inactivation compared to high-pressure processing associated with moderate heat treatment (600 MPa, 75 °C for 30 min) and to a conventional heat treatment performed at 75 °C for 30 min (Evelyn & Silva, 2015a).

On the other hand, thermosonication processing of soursop nectar did not promote differences in reducing gram-positive and gram-negative microorganisms. The highest lethality values were observed for Escherichia coli (5.16 log CFU/mL) and Staphylococcus aureus (5.18 log CFU/mL) using the same thermosonication treatment at 54 °C applying 1.4 W/mL for 10 min (Anaya-Esparza et al., 2017a, b). Logarithmic reductions in the E. coli count of 6.62 log CFU/mL were also observed in a pumpkin juice after thermosonication at 60 °C applying 150 W for 30 min (Demir & Kılınç, 2019). Yin et al. (2018) also reported reductions of 6 log cycles in the count of the microorganism responsible for the beer quality deterioration (L. acetotolerans). This study demonstrated that an energy density of 8.9 W/mL (24 kHz, ≥ 4 min, 40/60 °C) was needed to inactivate the exponential growth and cells in a viable but non-culturable (VPNC) state. Bacteria in VPNC state are unable to grow and develop in colonies in environments where they usually would. However, they are alive and capable of metabolic activity (Deng et al., 2015).

Other studies have reported lower reductions in the count of microorganisms. They have even assessed the additive effect of two emerging technologies on their inactivation. Thermosonication processing of apple juice reduced 2.7 log cycles in the E. coli count (400 W, 50 °C, 5 min, 8 mL/min). However, the combined heat treatment with pulsed light achieved decreases of up to 5.9 log cycles (Muñoz et al., 2012). Martínez-Moreno et al. (2020) observed that a thermosonication treatment applying pulsed ultrasound on soursop puree in the vacuum (16.5 kPa, 3 IVPs, 50 °C, 10 min) reached the highest values of inactivation of E. coli (7.58 log CFU) and S. aureus (7.35 log CFU).

Impact of Thermosonication Processing on the Enzyme Inactivation

Thermosonication has also promoted the inactivation of enzymes in food products, mainly in vegetables and beverages. Acoustic energy-based treatments can promote the denaturation of proteins by depolymerizing and changing the conformation of their tertiary structure. They also can promote obstructions in Van der Waals interactions and hydrogen bonds (Amador-Espejo et al., 2020). These obstructions are caused by the formation of free radicals in the sonicated medium, as related in the “Fundamentals of Ultrasound Technology” section. However, some enzymes may exhibit resistance to thermosonication processing, which may be associated with an intrinsic characteristic of the thermal resistance of the enzyme. Because of this, the most thermally resistant enzymes found in the food matrix are used for perform the thermosonication process design (Marques Silva & Sulaiman, 2017).

Amador-Espejo et al. (2020) evaluated the effects of thermosonication treatment in a fruit smoothie. The increase of ultrasound amplitude decreased the activity of pectin methylesterase (PME). On the other hand, the polyphenol oxidase (PPO) activity decreased using longer treatments. The thermosonication treatment carried out at 77.5% of amplitude, and 47.5 °C for 20 min resulted in PPO and PME activities of 4.82 and 0.12 UEA/mL, respectively.

The inactivation of PPO was also observed in pitaya juice. A PPO residual activity of 2.17% was observed after the treatment performed at 50 °C applying 380 W for 20 min. The enzyme was inactivated by extending the holding time to 40 min (Liao et al., 2020). Baltacıoğlu et al. (2017) also studied PPO inactivation in mushroom suspensions (pH 6.5). They used a 3-mm diameter probe at 24 kHz with 400 W in the amplitudes of 60, 80, and 100%. The inactivation kinetics was evaluated from 5 to 30 min using the working temperatures from 20 to 60 °C. The results showed a significant decrease in the PPO residual activity with increased ultrasonic power, temperature, and holding time. A PPO inactivation higher than 99% was observed after the treatment carried out at 60 °C with an amplitude of 100% for 10 min. The PPO inactivation by thermosonication occurred due to the irreversible alteration in the secondary structure of the enzyme.

Raviyan et al. (2005) studied the inactivation of PMEs in tomato suspensions (pH 7.5). They used a 13-mm diameter probe operating at 20 kHz by applying 750 W in the amplitude of 20 µm. The working temperatures were 61 °C and 72 °C. The temperature rise favored the PME inactivation. The highest PME inactivation regarding D value was obtained after treatments at 61 °C for 0.8 min and at 72 °C for 0.3 min. PME activity was also reduced by 90% in tomato juice (24 kHz, 25–75 μm). The exposure time to heat significantly affected the inactivation of this enzyme. Otherwise, the use of different amplitude levels did not promote a significant effect. Additionally, the working temperatures of 60 °C and 65 °C resulted in a higher PME inactivation. These temperatures reduced the enzyme activity by about twice as much as 70 °C. The authors explained that this higher temperature might have increased the vapor pressure cavitation bubbles. In this way, the working temperature of 70 °C may have favored the damping effect, reducing the acoustic cavitation intensity (Wu et al., 2008). Terefe et al. (2009) also observed a decrease in the PME inactivation rate by increasing the working temperature from 60 to 75 °C. They studied the thermosonication processing at 20 kHz and 75 μm of tomato juice. The PME inactivation rate was 6 and 1.5 times for treatments performed at 60 and 75 °C, respectively. Although the PME inactivation was low, applying working temperatures of 70 and 75 °C, these were 3.9 and 1.4 times higher than the inactivation of thermal treatments performed at the same temperatures. The discrepancy in the results obtained in the two studies presented may be associated with the variety of tomatoes, the process conditions, such as the differences in the sonotrode geometry and energy density applied. The energy density applied in the first study was 0.48 W/mL, while in the second was 1.6 W/mL. The PME and peroxidase (POD) activities were also evaluated by Pinheiro et al. (2016) in whole tomatoes. A thermosonication treatment at 40 °C and 45 kHz for 30 min resulted in a PME inactivation of only 25%. Furthermore, a gradual increase in PME activity occurred throughout the cold storage at 10 °C. The thermosonication promoted a different effect on the POD activity. The thermosonication increased POD activity by 26%. After that, its activity was reduced throughout storage. On the other hand, a thermosonication treatment at 51 °C applying 1.4 W/mL for 10 min reduced the PPO activity by 99% in soursop nectar. Besides that, no PPO activity was detected during the storage (Anaya-Esparza et al., 2017a, b). Thus, thermosonication treatments using higher temperatures may favor the PPO inactivation. Additionally, the product’s intrinsic characteristics of the product on which the treatment is applied can affect enzyme inactivation.

Critical Observations

The process standardization applied to food products is crucial to ensure the safety and quality of foods and beverages, mainly when innovative technologies are introduced to the manufacturing process. Furthermore, the scaling up of the thermosonication process for industrial lines depends on its standardization. However, some inconsistencies were verified in the thermosonication methodologies. The application of low-frequency ultrasound in a liquid medium provides heat due to the phenomenon of acoustic cavitation, as previously discussed. The cavitation bubble explosion releases high energy promoting the homogenization of the liquid medium and temperature rise. In this way, the energy provided to sonication modulates the acoustic cavitation intensity and, consequently, the temperature increase. Since thermosonication treatment is based on the combined action of acoustic energy with a mild heat treatment, monitoring the total thermal energy supplied for the system is fundamental for understanding the actual heat impact of the heat on thermosonicated foods products. Thus, the monitoring of thermal histories of thermosonicated samples is recommended, or at least the temperature differentials before and after thermosonication processing. Many studies did not report the temperature changes throughout thermosonication treatments. They studies have reported only working temperatures. In other words, they are only reporting the heat supplied by the external heat source. Thus, the actual heat treatment to which the thermosonicated samples were subjected was omitted (Almanza-Rubio et al., 2016; Avila-Sosa et al., 2010; Erkaya et al., 2015; Evelyn & Silva, 2015b; Fan et al., 2019a, b; Gursoy et al., 2016; Illera et al., 2018; Inmanee et al., 2020; Jabbar et al., 2015; Kassem et al., 2018; Khaire & Gogate, 2018; Liao et al., 2020; Lv et al., 2019; Pennisi et al., 2020; Pinheiro et al., 2016; Pinheiro et al., 2019).

Some studies have monitored the temperature during thermosonication treatment. Riener et al. (2009, 2010) observed that samples 75 °C after 6 min in a thermosonication process which set a working temperature of 45°C. Samples processed in bath-type ultrasound presented a lower temperature rise. The greater heat exchange area of bath-type ultrasound equipment contributes to energy dissipation in heat form, reducing the system temperature. In this type of ultrasound equipment are observed increases from 1 to 4 °C in the working temperature (Martínez-Moreno et al., 2020; Milani & Silva, 2017; Yin et al., 2018). Other studies also stated the need to set 2 or 3 °C below the working temperature to avoid overheating throughout thermosonication treatments at 50 to 75 °C (Terefe et al., 2009; Wu et al., 2008). In contrast, other studies have ensured that the process temperature was similar to working temperature (40, 50, 60, 55, 75, and 85 °C) throughout the treatment (Demir & Kılınç, 2019; Deng et al., 2018; Fan et al., 2020; Haughton et al., 2012; Hooshyar et al., 2020; Piao et al., 2019; Walkling-Ribeiro et al., 2009).

The keyword “thermosonication” has also been associated with processes that did not use an external heat source to maintain constant working temperature. These studies used only the heat provided by sonication. Goat’s milk samples, for example, were previously pasteurized at 72 °C for 15 s and then sonicated in an ice-coated beaker (Ragab et al., 2019). Amador-Espejo et al. (2020) also heated samples of fruit smoothies to 40 or 55 °C previously to thermosonication. However, the working temperature was not maintained by an external heat source throughout the treatment. Other studies established working temperatures of 40 and 50 °C but used water recirculation baths at 10 or 23 °C (Muñoz et al., 2011, 2012). Cold-water recirculation was also used in a thermosonication treatment (Halpin et al., 2014; Križanović et al., 2020). Ribeiro et al. (2017) sonicated samples of coconut water at room temperature without the aid of an external heat source. The thermal histories of this study demonstrated an increase in the sample temperature from 23 to 80 °C throughout sonication time. Blueberry juice samples, treated in the same way, presented an increase in their temperature from 17 to 70 °C due to increased processing time (Režek Jambrak et al., 2017). From the point of view of most studies on thermosonication processing examined in this review, the thermosonication treatment must be performed by combining acoustic energy with an external heat source to maintain the working temperature. However, inconsistencies in the process methodology may be solved with the own name of this emerging technology, which defines the application of ultrasound and heat simultaneously.

Conclusion and Perspectives

Thermosonication has shown promise for the inactivation of microorganisms and enzymes in foods and beverages, providing them lower impact on their nutritional and sensory quality compared to severe thermal treatments. Furthermore, the undesirable effects of this emerging technology on the quality aspects of food products can be minimized by modulating thermosonication process conditions. On the other hand, many treatments even increased the availability and retention of bioactive compounds in foods and beverages, including throughout their storage.

Thermosonication has been widely studied in the processing of fruit and vegetable juices. However, few studies have been performed to evaluate thermosonication effects on meat and dairy products and fermented beverages. In this way, there is a demand for more studies about these food groups.

Depending on the thermosonication process design, high thermal energy may be delivered to food products due to the coupled treatment between sonication and heat by an external source. Therefore, the monitoring of thermal history throughout the processes is a crucial requirement to achieve the aims set for the process. Monitoring thermal history ensures the maintenance of food quality and safety.