Recent advances of ultrasound-assisted Maillard reaction

Ultrasonics - Sonochemistry xxx (xxxx) xxxx

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Recent advances of ultrasound-assisted Maillard reaction ⁎

⁎

Hang Yua,b,c, , Qili Zhonga,b,c, Yang Liua,b,c, Yahui Guoa,b,c, Yunfei Xiea,b,c, Weibiao Zhoud, , ⁎ Weirong Yaoa,b,c, a

State Key Laboratory of Food Science and Technology, Jiangnan University, No.1800 Lihu Avenue, Wuxi, Jiangsu Province 214122, China School of Food Science and Technology, Jiangnan University, No.1800 Lihu Avenue, Wuxi, Jiangsu Province 214122, China Joint International Research Laboratory of Food Safety, Jiangnan University, No.1800 Lihu Avenue, Wuxi, Jiangsu Province 214122, China d Department of Food Science and Technology, National University of Singapore, 3 Science Drive 3, Singapore 117543, Singapore b c

A R T I C LE I N FO

A B S T R A C T

Keywords: Ultrasound Maillard reaction Kinetic model Flavor generation Protein glycation Food processing

Maillard reaction (MR) is one of the most important chemical reactions in the food science domain with a long history of more than 100 years. As for ultrasound-assisted MR (US-MR), it has gradually drawn attention in a recent decade. Purpose of this paper is to provide a systematic review on recent advances of US-MR in model systems, glycation of protein, and food processing. Fundamental studies on simple MR model systems (i.e. reducing sugar and amino acid) have reported a promoted generation of colored and volatile MR products (MRPs). Critical steps influenced by US and possible mechanisms have been elucidated simultaneously. Other studies focused on modification of proteins which undergoes a glycation between proteins and saccharides as the initial stage of MR. Since the MR rate is extremely low in the presence of protein and saccharide, US becomes a promising mean of promoting the glycation. As a result, a number of functional properties of glycated protein obtained by US are significantly promoted, which extend their utilization in the food industry. The rest of studies reviewed in this article are concentrated on applying US to process real foods. Many attributes changed during US-assisted processing are induced by MR. Positive aspects brought by the promoted US-MR include enhanced antioxidant capacity and organoleptic properties (e.g. desirable color, low bitterness, enhanced flavor, etc.), as well as inhibited hazards (e.g. advanced glycation end-products, acrylamide, etc.) formed in the processed foods. Meanwhile, the promoted MR by US may also inevitably bring some negative aspects to the processed foods due to unfavored yellowish/browning colors, off-flavors and hazard components.

1. Introduction The use of ultrasound (US) processing in the food industry is a relatively new endeavor compared with conventionally mechanical and thermal processing. Homogenization, extraction, inactivation of enzymes and microorganisms, etc. with assistant of US have been adopted for food processing purposes [1]. In a recent decade, effects of US on Maillard reaction (MR) have gradually drawn attention in the food science domain. As one of the most important chemical reactions in the

food systems, the MR generates important and distinctive MR products (MRPs) during food processing. US as an emerging technology, therefore, is expected to promote positive but inhibit negative attributes brought by the MR. A number of food-grade proteins are considered as valuable nutritional sources. For improving solubility, stability and emulsification of proteins under unfavorable aqueous pH conditions, a direct conjugation with various mono-, di-, and poly-saccharides (e.g. glucose, sucrose, maltodextrin, etc.) is considered as a promising strategy. One of

Abbreviations: AGEs, advanced glycation end-products; BLG, β-Lactoglobulin; BPI, buckwheat protein isolate; BSA, bovine serum albumin; CEL, NƐ-(hydroxyethyl) lysine; CML, NƐ-(carboxymethyl)lysine; CUPS, continuous ultrasonic processing system; CUTR, continuous ultrasonic tank reactor; DG, degree of graft; 1-DG, 1deoxyglucosone; 3-DG, 3-deoxyglucosone; Ea, activation energy; 2-FM-Arg, 2-furoylmethyl-arginine; 2-FM-Lys, 2-furoylmethyl-lysine; G’, storage modulus; H0, surface hydrophobicity; HMF, 5-hydroxymethylfurfural; MG, methylglyoxal; MMPH, mussel meat protein hydrolysate; MR, Maillard reaction; MRPs, Maillard reaction products; MPI, mung bean protein isolate; OVA, ovalbumin; PEG 6000, polyethylene glycol with a molecular weight of 6000; PPI, peanut protein isolate; RANS, Reynolds-averaged Navier-stokes; SM, response surface methodology; SHVPH, smooth hound viscera protein hydrolysates; SPI, soybean protein isolate; US, ultrasound; US-MR, ultrasound-assisted Maillard reaction; WP, whey proteins; WPI, whey protein isolate; WPP, whey protein peptide ⁎ Corresponding authors at: State Key Laboratory of Food Science and Technology, Jiangnan University, No.1800 Lihu Avenue, Wuxi, Jiangsu Province 214122, China (H. Yu and W. Yao); Department of Food Science and Technology, National University of Singapore, 3 Science Drive 3, Singapore 117543, Singapore (W. Zhou). E-mail addresses: [email protected] (H. Yu), [email protected] (W. Zhou), [email protected] (W. Yao). https://doi.org/10.1016/j.ultsonch.2019.104844 Received 10 September 2019; Received in revised form 30 September 2019; Accepted 25 October 2019 1350-4177/ © 2019 Elsevier B.V. All rights reserved.

Please cite this article as: Hang Yu, et al., Ultrasonics - Sonochemistry, https://doi.org/10.1016/j.ultsonch.2019.104844

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of acoustic energy; upon reaching a critical size, the cavities would implode, release energy and heat to the surroundings reaching up to an extraordinarily high temperature of about 5,500 °C, followed by a flash cooling at the rate of more than a billion °C/s [20]. Hence, the cavitation generated by high-intensity US brings a unique environment for chemical reactions [21,22]. Sound waves are also considered as a safe, non-toxic, and environmentally friendly processing method, which gives the use of US a major advantage over other emerging techniques [1]. Different intensity and frequency of US would have different applications. Low-intensity US (less than 1 W/cm2) with the frequency range of 1–10 MHz is utilized as a nondestructive detection method; it has already been utilized in food process control and characterization of food properties. At higher frequencies (> 1 MHz), acoustic pressures are lower, and this amplitude is more readily dissipated within the fluid. For lower frequency-high intensity US, it is much easier to generate an acoustic wave of high amplitude and acoustic pressure making it suitable as a mean of processing. It is worth noting that high-intensity US (from 1 to 1000 W/cm2) is able to expand the cavities much faster than low-intensity US, which has drawn much attention in the food science domain. Currently, high-intensity US with the lower frequency range of 20–100 kHz has been treated as an alternative to conventionally thermal processing due to its low energy consumption, as well as the reduction of processing time and thermal effects [23,24]. As an emerging technology, high-intensity US has some existing applications in food processing, e.g. US-assisted cutting, sterilization, extraction, drying, freezing, etc. [25]. It is also a potential candidate for producing foods with modified properties, e.g. stabilization of whey protein, enhancement of flavor generation, etc. [26,27].

practical ways to achieve grafting of protein is through the MR under controlled conditions [2–4]. The rate of MR between protein and saccharide is extremely low. Possible reason includes compact quaternary and tertiary structures of proteins that protect reactive amino groups. These structures make grafting of proteins hard to be conducted through the MR; therefore, this procedure normally requires a high processing temperature and extended reaction duration (usually takes several days) [5]. US as an alternative strategy would be a suitable candidate for promoting the glycation of proteins through the MR. The colored MRPs generated during heat treatment, e.g. melanoidins, are welcomed in certain food products; for example, many of bakery products with desired browning color, like cookies and bread, always impress consumers as high-quality and attractive products [6]. Besides colored MRPs, it is also important in the generation of flavor compounds as final MRPs. For example, roasting cocoa bean generates a number of characteristic and desirable volatile compounds with roasted flavors through the MR, which are favored by consumers [7]. The MR is one of the most powerful pathways to synthesize commercial flavor products by the food flavor industry, such as furans, pyrroles, pyridines, pyrazines, thiophenes, etc. [8]. Studies on US-assisted MR (US-MR) in glucose-glycine model system would generate more flavoring compounds with lower odor thresholds and higher concentration [9,10]. In addition, a number of MRPs contribute to increased antioxidative and antimicrobial capacities, as well as high-value nutritional and physical properties of products that can be generated with assistance of US [11]. Therefore, the generation of desirable MRPs are expected to be promoted throughout the US-MR during food processing. There are also some negative effects brought by the MR. As for the browning caused by the MR, it is normally inevitable but not always desirable in food products. For example, the generation of melanoidins should be minimized during heat treatment of dairy products to produce the final products with a natural color; meanwhile, the MR should be properly controlled in order to preserve high-valued nutrients in the dairy products, e.g. essential amino acids and peptides [12,13]. Offflavors and undesirable MRPs may be released via the MR during food processing and throughout further storage period. An example of generating acrylamide as one of carcinogenic MRPs in a food system containing reducing sugars and asparagine through the MR should be prevented [14]. As reported in Gao, Zheng and Chen [15], US-MR would be accelerated asparagine-glucose MR model system without acrylamide formation, which is considered as a safer technology compared with the thermal treatment. Advanced glycation end-products (AGEs), including furosine, pyrraline, NƐ-(carboxymethyl)lysine (CML), NƐ-(hydroxyethyl) lysine (CEL), etc., refer to a group of structurally complex and chemically stable end products produced at the final stage of MR, and some of which are proved to trigger chronic vascular diseases [16–18]. Therefore, it is worth studying and adopting interventions to control the MR in these scenarios. For now, there is no comprehensive review concentrating on the USMR. The significances of this review include: 1) revealing critical steps of US-MR promoted/inhibited by US in model systems; 2) summarizing US-assisted glycation of proteins with improved functional properties compared with those obtained by conventionally thermal treatment; 3) concluding attributes and properties related to the MR occurred in USprocessed foods.

3. Maillard reaction The MR is a non-enzymatic browning reaction between reducing sugars and amino acids, peptides or proteins, which has been studied for over a hundred years since French chemist Louis-Camille Maillard first reported about the MR in 1921. The MR commonly occurs during thermal food processing; however, contrary to conventional believe, the MR can also occur at relatively low temperatures, e.g. during storage at room temperature. So far, previous studies have demonstrated that the reaction rate of MR is dependent on various conditions, e.g. combination and types of reactants, concentration of reactants, initial pH, water activity, reaction temperature, reaction time, etc. [28,29]. Among the above-mentioned conditions, the types of reactants highly determine the rate of MR. For example, the rate of MR is inversely proportional to the size of the reducing sugar molecule. For example, pentoses have been proved to react faster than hexoses [30]. The chemical structure of the amino acid reactant is another determining factor on the reaction rate. Lysine has two reactive non-ionized amino groups (–NH2) that easily catalyze fragmentation of reducing sugars; therefore, it has a higher reactivity compared with other amino acids [9]. Generally speaking, the types of reactants majorly influence the flavor profile generated from the MR, and the rest of conditions determine the kinetics of MR [31]. Hodge [32] first described the principle of reaction steps involved in MR. The reaction is initiated by the condensation between a carbonyl group of reducing sugar and an amino compound, and subsequently produces the Schiff base. The Schiff base can be further converted to Amadori and Hyens compounds depending on the presence of aldoses and ketoses, respectively [33]. The Amadori and Hyens compounds simultaneously undergo deamination, dehydration and fragmentation to generate final MRPs with one or more carbonyl groups, such as furfurals, furanones, pyranones, etc. Due to their instability above the ambient temperature, the Amadori and Hyens compounds rapidly undergo enolisation, release amino groups, and generate 1,2-enaminol and/or 2,3-enaminol depending on the pH condition. Both 3-deoxyosone (3-DG) and 1-deoxyosone (1-DG) are dicarbonyl compounds

2. Ultrasound US is defined as any sound with its frequency above 20 kHz, which is beyond the threshold of human hearing [19]. Passing US wave through the targeted media results in a continuous wave-type motion. The motion creates two of alternative cycles, namely compression and expansion. In a liquid, cavities are generated during the expansion cycle due to a large negative pressure overcoming the liquid’s tensile strength; the compression cycle generates positive pressure, which can push molecules together. The cavities keep growing with the absorption 2

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higher than the thermally processed sample at the same temperature level. The generation of colored MRPs is generally promoted in the USMR model systems except for xylose-lysine [9]. This phenomenon can be explained as follows: the generation of colored and volatile compounds as final MRPs are the two competitive reaction pathways. The amino groups in lysine would impart into the Strecker degradation for the flavor generation. Since lysine as the most reactive amino acid contains two available α- and ε- amino groups, it is possible that higher proportion of intermediate MRPs impart into the Strecker degradation instead of the generation of colored MRPs; therefore, leading to a decreased generation of colored MRPs in lysine-xylose MR model system. Besides the MR, promoted isomerization was also observed in a lactoselysine MR model system which converts the lactose to lactulose. The US assistance during the isomerization of lactose achieved a 34.5% increase in concentration of lactulose than that treated by thermal MR without US [38]. As one of the distinctive chemical effect in aqueous systems, cavity implosion during US application is high enough to decompose water into H• and •OH radicals with extremely high reactivity. During the lactose isomerization, these free radicals generated by US might favor the oxidation of intermediate compounds making them possibly been trapped by the ions carbonate and bicarbonate, therefore, increase the formation of lactulose through the isomerization [39]. Sulfur-containing amino acids, e.g. cysteine and methionine, are important raw materials for synthesizing meaty flavors through the MR. A previous study was conducted to optimize US processing conditions in a MR model system of xylose-cysteine through response surface methodology (RSM) [40]. Taking 2-methylthiophene and tetramethyl pyrazine as target flavor compounds, the processing condition was optimal at pH of 6.00 accompanied with 78.1 min of US processing at the intensity of 19.8 W/cm2. As an emerging technology for promoting the generation volatile MRPs through the MR, degassing effect of US is fatal for expulsion of generated food flavors. An improvement of experimental set-up was made in a subsequent study on MR model system of glucose-methionine, which designed a continuous ultrasonic tank reactor (CUTR) and adopted a continuous ultrasonic processing system (CUPS) in order to largely keep the flavors and minimize negative aspects brought by the US degassing effect [35,41]. It was reported that final concentration of methional in US-MR was about 3 times higher than that in the thermal one at the same temperature, which again proved the high efficiency of keeping volatile MRPs in the US-MR model system of glucose-methionine [35]. The design of CUTR and CUPS will be introduced in Section 4.3. Kinetic modelling is one of powerful tools on studying mechanisms and revealing potential reaction pathways of MR which are promoted/ inhibited by US. One of the most comprehensively kinetic studies was conducted by Yu, Seow, Ong and Zhou [36] on a US-MR model system of glucose-glycine. As shown in Fig. 1, reaction scheme of MR was largely divided into four stages. Activation energy (Ea) of glucose isomerization in the US-MR was determined to be 100.8 kJ/mol, which was 19.7% higher than that required by the thermal one. This phenomenon is explained as follow: when the MR was promoted by US, and the isomerization of glucose, therefore, was suppressed as a competitive reaction against the MR. In addition, intermediate stage of MR was significantly promoted by US. As a result of the promotion, Ea value required by generation of 1-DG in the US-MR was about 40% lower than that required by the thermal counterpart. Due to a significantly higher concentration of 1-DG, formation of all final MRPs selected in this study were promoted, including colored and volatile MRPs. In particular, two unique pyrazines, i.e. 3,5-diethyl-2-methylpyrazine and 3,5-dimethyl-2-vinylpyrazine, were only detectable in the US-MR samples, but absent after thermal processing. This phenomenon would be attributed to the high pressure-favored aldol-type condensation, which was promoted by a high-pressure environment generated by US. Moreover, similar studies were conducted to compare US-MR and thermal MR in model systems of xylose-lysine, glucose-serine, and glucose-methionine [9,35,42]. In the MR model system of glucose-

and identified as intermediate MRPs, which are converted from 1,2enaminol and 2,3-enaminol, respectively. The generation of 3-DG tends to be promoted via 1,2-enolization in acidic conditions; meanwhile, the conversion into 1-DG via 2,3-enolization is suppressed. With an increased pH condition, the generation of 3-DG is suppressed, but that of 1-DG is promoted [34]. With the reaction proceeding, the dicarbonyl compounds are able to react with amino-containing compounds again, and subsequently generate colored MRPs [35]. The Strecker degradation is another important reaction pathway associated with the generation of volatile MRPs. The Strecker degradation starts between amino acids and α-dicarbonyl compounds, in which the amino acids are decarboxylated and deaminated to yield Strecker aldehydes and αamino ketones [36]. The α-amino ketones are the most important precursors of alkylpyrazines as an important group of volatile MPRs. The generation of alkylpyrazines starts from the self-condensation of the α-amino ketones. Other heterocyclic compounds, such as oxazoles and thiazoles, can also be generated from the α-amino ketones [8]. Therefore, Strecker degradation products and carbonyl compounds formed through intermediate MRPs provide distinctive flavor compounds through the MR. 4. Ultrasound-assisted Maillard reaction in model systems For now, many food scientists have conducted a serial of fundamental studies on US-MR in model systems. Among these, most of researches have observed many changes on depletion of reactants, generation of colored and volatile MRPs, as well as antioxidant capacity in MR model systems as summarized in Table 1. 4.1. Simple Maillard reaction model systems with assistance of ultrasound The very first study on US-MR model system was glucose-glycine, which is one of the simplest MR model system [10]. After adopting different intensity levels of US ranging from 10.19 to 17.83 W/cm2, significant increases on depletion of reactants, generation of intermediate and colored MRPs, as well as reducing power and DPPH-radical scavenging activity of MRPs were observed. In addition, generation of organic acids as final MRPs is another indicator for the extent of MR. A fast dropping of pH value from 11.0 to 8.2 within 50 min with high-intensity US treatment at 17.83 W/cm2 was observed; however, only a fluctuation of pH value was detected with US treatment at 10.19 W/cm2. Based on results of GCMS analysis, ester and pyrazine as favorable MRPs were more possibly to be generated at 17.83 W/cm2, and major flavor compounds were identified as trimethyl-pyrazine, 2,5dimethylpyrazine, 1,2-benzenedicarboxylic acid, (Z)-9-octadecenamide, and mono (2-ethylhexyl) ester. Another similar study on US-MR model system of maltose-glycine has reported similar findings. Therefore, authors concluded that high-intensity US could potentially be applied as a means of promoting the MR with the intensity higher than 15.29 W/cm2 [37]. With the proceeding of studies on L-lysine based US-MR model systems involving xylose, glucose, and lactose, changes on more types of intermediate and final MRPs were determined and compared with their thermally processed counterparts. As reported in Yu, Seow, Ong and Zhou [9], US-MR (frequency: 20 kHz, intensity: 11.90 W/cm2) would promote a critical MR step named aldol-type condensation, which enables forming more complex volatile MRPs with more/longer side chains compared with the thermal MR at the same temperature level, e.g. 3-ethyl-2,5-dimethylpyrazine, butyl amine, and maltol. The aldol-type condensation is considered as a pressure-favored reaction, which is promoted under an extremely high, albite momentary, pressure and temperature environment generated by US. In a glucose-lysine MR model system, initial step of MR was significantly promoted after the US treatment (frequency: 20 kHz, power: 400 W) through determining 2-duroylmethyl-lysine (2-FM-Lys) as an indicator of initial stage of MR. The concentration of 2-FM-Lys in the US-MR was 19.4% 3

4

3

2

1

55, 60, 65, 70, 75 °C

20 kHz

D-glucose-L-serine

2

20 kHz

D-glucose-L-methionine

55, 60, 65, 70, 75 °C 70, 80, 90 °C 0–120 min

0–90 min

0–120 min

0–90 min

60 min

–

–

–

↓5.38% of D-glucose 1; ↑15.8% of fructose 2; ↓ 2.54% of L-alanine ↓5.38% of D-glucose; ↑ 18.5% of fructose

↓69.4% of 1-DG; ↓ 80.5% of MG –

↓101.6% of 2, 5-dimethylpyrazine; ↓40.4% of 3-ethyl-2,5dimethylpyrazine

–

–

↓30.9% of D-xylose; ↓ 12.4% of L-lysine ↑19.7% of fructose ↓39.6% of D-glucose; ↓ 34.27% of L-serine

↓12.5% of 2,5-dimethylpyrazine; ↓31.5% of 2,3,5trimethylpyrazine; ↓34.9% of 3-ethyl-2,5-dimethylpyrazine; ↓25.7% of 2,3,5,6-tetramethylpyrazine; ↓23.9% of melanoidins ↓13.0% of 2,3,5-treimethylpyrazine

↓74.1% of 1-DG

↑46.7% of 2,3,5-trimethylpyrazine; ↑738.9% of 2,3,5,6tetramethylpyrazine

↑300% of methional; ↑27.3% of A420 value 37 and 25 volatile compounds detected in US-MR and thermal MR ↑50.1% of formic acid;

↑176.9% of A420 value

↓32.7% of A420 value

Final stage of MR

↑19.7% of fructose

–

↑11.9% of 2-FM-Lys

–

3

–

Intermediate stage of MR

–

Initial stage of MR

“↓” refers to a significantly lower concentration/Ea/absorbance value of the target compounds detected in US-MR and thermal MR; “↑” refers to a significantly higher concentration/Ea/absorbance value of the target compounds detected in US-MR and thermal MR; “–” refers to not detected the compound in this study.

11.90 W/cm

11.90 W/cm

2

11.90 W/cm2

20 kHz

D-xylose-L-lysine

70, 80, 90 °C

11.90 W/cm2

20 kHz

Ea of reaction steps

80 °C

11.90 W/cm2

20 kHz

60 min

80 °C

11.90 W/cm2

20 kHz

D-glucose-L-alanine (with canola/olive/ palm/coconut oils) D-glucose-glycine (with sunflower/peanut/ olive/flaxseed oils) D-glucose-glycine

0–90 min 78.1 min

70, 80, 90 °C 60 °C

20 kHz 20 kHz

D-glucose-L-methionine D-xylose-L-cysteine

15, 30, 60 min

0–120 min

400 W (amplitude 50% and 70%) 11.90 W/cm2 19.8 W/cm2

20 kHz

D-glucose-L-lysine

11.90 W/cm

55, 60, 65, 70, 75 °C 25, 40, 60 °C

20 kHz

D-xylose-L-lysine

Concentration of target compounds

2

Reaction time

Temperature

Frequency

Intensity/power

Reaction conditions

US conditions

MR model systems

US-MR compared with thermal MR

Table 1 Comparisons on concentration of compounds and Ea of reaction step between US-MR and thermal MR in model systems.

[42]

[35]

[9]

[36]

[44]

[27]

[35] [40]

[38]

[9]

Refs.

H. Yu, et al.

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Fig. 1. Proposed reaction scheme of US-MR model system of glucose-glycine based on [36]; “↑” or “↓” refer to the step which is promoted or inhibited by US, respectively.

influence on the overall flavor profile due to different solubility. Another study was conducted on evaluating effects of US on glucose-alanine MR model systems with four oils with different saturations, i.e. canola, olive, palm, and coconut oils [27], and similar findings were reported as the previous one. Furthermore, this study has revealed impact of unsaturation degree of oils on the generation of volatile MRPs in the water phase. Results showed that formation of pyrazines with shorter side chain was significantly promoted in the presence of oils with a lower degree of unsaturation e.g. 2,5-dimethylpyrazine and 2,6-dimethylpyrazine. In turn, the oils with higher degree of unsaturation would suppress the generation of the shorter side chain pyrazines, but promoted the formation of pyrazines with longer side chains, e.g. 2,3-diethyl-5-methylpyrazine and 3,5-diethyl2methylpyrazine. As elucidated previously, such a difference on the formation of pyrazines was mainly attributed to the differences on carbonyl compounds generated through the lipid oxidation from different oils. Although some off-flavors may also form in the oil phase due to the promoted oxidation of oils by US, most of them were largely dissolved into the oil phase instead of water phase due to different solubility; therefore, it only had very limited impact on overall flavor profile of the water phase where the MR mostly happed. Therefore, the US-assisted oil-in-water MR model systems provided an alternative strategy for the generation of food flavors.

methionine, US was found to be significantly promoted the generation steps of 1-DG and MG, which achieved 69.4% and 80.5% increases in corresponding Ea values compared with those in thermal MR, respectively. In the xylose-lysine and glucose-serine MR model systems, combination of reducing sugars and amino acids as the initial stage of MR was significantly promoted by US as well. In general, all the studies on MR model systems have reported the promotion of MR brought by US. Most of the studies observed a promoted combination between reducing sugars and amino acids as the initial stage in US-MR. In addition, promoted generation of dicarbonyl compounds, including 1-DG, 3-DG and methylglyoxal (MG), were reported in many of US-MR model systems. As a result of promoted generation of dicarbonyl compounds, concentration of final MRPs, including colored and volatile compounds, were generally higher in USMR than those in thermal MR. One of unique phenomena reported in the MR model system is more types of volatile MRPs were formed with assistant of US. For example, pyrazines with longer/more side chains were only formed in the US-MR model system but absent in the thermal one. Based on previous study on odor threshold of pyrazines, it is indicated that odor threshold would be decreased after replacing one or more methyl-groups to ethyl-groups, or attaching longer side chains [43]. For example, 2-ethyl-3,5-dimethylpyrazine has the lowest odor thresholds (0.04 ± 0.01 μg L−1 in water and 0.011 ± 0.003 μg m−3 in air) among ethyldimethylpyrazines, which are 250 times lower than that of 3-ethyl-2,5-dimethylpyrazine and thousand times lower than that of 5-ethyl-2,5-dimethylpyrazine. Therefore, these pyrazines largely synthesized in US-MR would lower down odor threshold of flavors with higher commercial value. US processing would also increase antioxidant capacity and reducing power of MRPs since a number of MPRs contribute to relatively strong antioxidant activity.

4.3. Design of continuously ultrasonic processing system for producing flavors through ultrasound-assisted Maillard reaction In order to largely keep volatile MRPs formed in US-MR sample and minimize loss of flavors caused by degassing effect of US, the CUTR and CUPS were adopted, as shown in Fig. 2A and B, respectively. In general, the CUTR is assembled by four parts, i.e. an ultrasonic probe, an inner reactor, a highly thermal-conductive layer and a cooling water jacket layer (Hielscher, Germany). The cooling water jacket covers more than 80% of total surface of inner reactor making it efficiently taken away many heats generated during US processing. An enforcement of highly thermal-conductive layer is used for bottom layer as well as side and upper layers of CUTR with thickness of 0.60 and 0.70 cm, respectively. Such a design is able to endure high pressure up to 10 bar during US processing. A further simulation of acoustic pressure and temperature in CUTR was conducted based on Reynolds-averaged Navier-stokes (RANS) k-ε equation, Helmholtz equation, and heat transfer models. Based on the results, the average core acoustic pressure reached to 414 atm during compression and expansion cycle when the output US intensity was determined to be 11.90 W/cm2. The temperature distributions were varied based on residence time of sample solution. For example, the highest average core temperature reached to 364.1 and 79.6 °C when the residence time was set to 120 and 15 min,

4.2. Oil-in-water Maillard reaction model systems with assistance of ultrasound It is the first time to report effects of US treatment on oils-in-water MR model systems for simulating real food processing conditions in the presence of edible oils. A US-MR model system of glucose-glycine with sunflower, peanut, olive and flaxseed oils was first studied in [44]. It was observed that both lipid oxidation and MR were significantly promoted by US. As a consequence of promoted lipid oxidation by US, some off-flavors were generated in the oil-phase; meanwhile, reactive carbonyl compounds as a part of lipid oxidation products were extensively formed and further imparted to MR as intermediate compounds, hence increased the MR where happened in the water phase. Higher concentration of desired flavor compounds in the water phase after US processing was significantly increased compared with the thermal one. The off-flavors in oil phase would only have a very limited 5

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Fig. 2. Design of (A) CUTR and (B) CUPS for food flavor generation through US-MR according to [9,41].

involves incubating the mixture of protein and saccharide at controlled temperature and relative humidity for a long period (up to several weeks). Such a long-time baking may result in a serious browning, and make the extent of reaction become uncontrollable [48]. Therefore, the dry-heating treatment is unattractive in the industrial viewpoint. Compared with the former one, the wet-heating treatment involves a thermal treatment of mixture in a buffer system. The even contact between reactants would accelerate the MR and reduce the reaction time to several days. However, due to very low reactivity of both reactants, the glycation between target protein and saccharide is still a timeconsuming and high temperature-required reaction [49]. Moreover, denaturation and aggregation of protein may occur at the high temperature and long duration, which brings negative impacts on functionalities of the protein-saccharide conjugates [50]. Therefore, it is necessary to develop an emerging technology, i.e. US, to improve the efficiency of MR. For now, many applications on US-assisted glycation have been adopted and successfully achieved the glycation of various proteins through MR as summarized in Table 2.

respectively. Results of simulation study again indicated two typical consequences of US processing, including the extremely high-pressure cycle leading to agitation and turbulence , as well as the momentary high core temperature. Besides the CUTR, other essential parts of US generating system include ultrasonic generator, transducer, booster, probe, etc. The preprepared sample solution was always pumped from bottom of the reactor and flowed out at the top. The rest of essential parts of CUPS include cooling, pumping, collecting and monitoring systems. The cooling system keeps pumping cooling water through the cooling water jacket on the CUTR for maintaining temperature throughout US processing. The flow rate and temperature of cooling water will be properly controlled by the refrigerated bath circulator. The pumping system is responded to transport the pre-prepared sample solution into the CUTR (from bottom to top) at different flow rate via changing rotation rate of a peristaltic pump. As for monitoring system, temperature sensors are inserted into the both inlet and outlet of cooling water pipelines as well as the inner chamber of CUTR for monitoring and recording temperature changes of cooling water, initial and final temperature of processed sample. An establishment of collection system with a threeway valve conjugated among the pipelines of CUTR outlet, processed sample container and sample collector tube is able to collect processed samples. Such a design provides a relatively closed environment during US processing; therefore, it can largely keep the flavors generated through US-MR and minimize loss of flavors due to degassing effect of US.

5.1. Ultrasound-assisted Maillard reaction for modifying plant origin proteins/peptides Both soybean and mung bean are good sources of protein with a relatively high protein content ranging from 20 to 36% [51,52]. Soybean protein isolate (SPI) and mung bean [Vigna radiate (L.)] protein isolate (MPI) are widely used as plant origin emulsifiers or emulsion stabilizers in food formulations, e.g. meat emulsions, infant foods, and liquid diets [53,54]. As reported in Zhao, Zhou, Liu, Zhang, Chen and Wu [55], US-MR between SPI and glucose/maltose was first conducted with a heat treatment at 95 °C for 15 min followed by an US treatment at 25 kHz, 200 W for 20 min. Compared with the thermally treated sample without US, degree of glycation (DG) of SPI-glucose and SPImaltose were increased by 44.8% and 104.4%, respectively. It is possibly attributed to a rapid molecule movement caused by the cavitation and unfolding of protein chains during the US treatment, which allows reactive groups to bring into closer proximity. A further comparison on browning intensity between SPI-glucose and SPI-maltose showed that the SPI-maltose system had a significantly higher A420 value. Both increased DG and A420 values are indicators for the promoted MR between SPI and the two reducing sugars with the assistant of US [56]. Surface hydrophobicity (H0) refers to an index of hydrophobic

5. Glycation of proteins/peptides through ultrasound-assisted Maillard reaction A number of plant or animal origin proteins have high nutrition and various functions which make them extensively used in the food industry [45]. Functional properties of proteins are of important, e.g. solubility, emulsifying, gelling and foaming abilities, etc. Therefore, these functional properties need to be further improved through appropriate modifications, including physical, chemical and enzymatic treatments [46]. Among these, the MR is treated as a suitable method of modifying proteins through thermal processing without adding external chemicals [47]. There are two conventional ways to prepare protein-saccharide conjugates, i.e. dry-heating and wet-heating. The dry-heating treatment 6

7

Sucrose

Glucose, xylose

BSA

SHVPH

MMPH

2

MMPH-glucose, MMPHxylose

SHVPH-sucrose

BSA-glucose

OVA-xylose

BLG-glycoconjugates

WPI-galactose, WPPgalactose WP-arabinose

PPI-maltodextrin WPI-gum acacia

BPI-dextran

10 W/cm

2

10.19–17.83 W/

300 W, 150.7 W/

9.5 W, 135 W/

25 kHz, 300 W, 60 °C

20 kHz, cm2 20 kHz, cm2 25 kHz, cm2 25 kHz,

20 kHz, 200 W, 110 W/ cm2 20 kHz, 135 W/cm2

20 kHz, 250 W 25 kHz, 100–700 W

544.59 W/cm

2

20 kHz, 450 W

15 kHz, 100–400 W 20 kHz, 450 W

25 kHz, 200 W, 138.26 W/cm2

US conditions

40 °C, 40 min US pre-treatment, and 90 °C, 2 h thermal process US pre-treatment with heat treatment at 115 °C, 2 h, pH = 6.0

less than 60 °C, 30 min, pH = 10.0

55 °C, 0–50 min, pH = 8.0

up to 60 min US pre-treatment, and 90 °C, 120–180 min thermal process, pH = 8.0 60 min, pH = 8.0 with crowding agent (PEG 6000) 10–15 °C, 60 min, pH = 6.5

70 °C, 100 min; pH = 3.8, wet heat 50–90 °C, 40 min, pH = 7.0–12.0

70 °C, 80 min; pH = 7.5

80 °C, 20 min, pH = 7.0, wet heating

128.2% of α-helix;↑186.4% of β-sheet; ↓9.2% of β-turns; ↑30.5% of random coli; ↑52.7% of DG;↑29.2% of free amino acids;↓40.2% of bitter taste;↑415.4% of antioxidant activity Rich in meaty and seafood flavors but lower bitterness;↑5%-20% of antioxidant capacity

76% of BLG was modified to BLG-ribose with the highest DPPH radical scavenging activity and reducing power ↑61.5% of H0;↑141.0% of foaming ability;↑42.4% of foaming stability;

↑38.3% of DG;↑101.1% of H0;↑79.7% and ↑57.8% of emulsification activity and stability, respectively ↓51.1% of α-helix; ↑45.8% of random coli; ↑5.8% of H0;↓50.5% of droplet size ↑32.4% of DG;↓49.8% of droplet size ↑136.5% of DG;↑162.5% of H0;↑30.88% of solubility;↑11.1% and ↑41.7% of emulsifying abilities and stabilities, respectively ↑19.4% (WPI-galactose) of DG;↑93.2% (WPI-galactose) and ↑48.6% (WPPgalactose) of DPPH radical scavenging activity ↑128% of DPPH radical scavenging activity;↑54.1% of solubility

[74]

[73]

[72]

[71]

[69]

[26]

[68]

[2] [67]

[64]

[61]

[58] [51]

[55]

↑44.8% (SPI-glucose) and ↑104.4% (SIP-maltose) of DG ;↑37.0% (SPIglucose) and ↑25.1% (SIP-maltose) of H0;↓22.7% (SPI-glucose) and ↓5.1% (SIP-maltose) of particle size 2 ↑0.7% of DG;↑12.6% of free amino groups;↓260.9% of droplet size ↑24.7% of DG;↑69.9% of H0;↑33.3% of emulsifying abilities and stabilities

Room temperature, 20 min US, and 95 °C, 15 min heating, pH = 7.0 40–90 °C, 5–60 min, pH = 7.0 90 °C, 60 min, pH = 7.0, wet heating

Refs. 1

Promoted properties compared with thermally processed counterparts

Reaction conditions

“↑” refers to the attribute significantly promoted in the glycated protein processed by US-MR compared with that obtained by wet-heating without US; “↓” refers to the attribute significantly inhibited in the glycated protein processed by US-MR compared with that obtained by wet-heating without US.

Glucose

OVA

1

Glucose, galactose, lactose, fructose, ribose, and arabinose Xylose

BLG

Maltodextrin Gum acacia

PPI WPI

Arabinose

Dextran

BPI

WP

Glucose

MPI

Galactose

Gum acacia Maltodextrin

SPI Soy β-conglycinin

WPI, WPP

SPI-glucose, SPI-maltose

Glucose, maltose

SPI

SPI-gum acacia Soy β-conglycininmaltodextrin MPI-glucose

Generated conjugates

Raw materials

Table 2 Summary of US-MR for generating protein-saccharide conjugates with promoted properties compared with their thermally processed counterparts.

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US. One improvement in [61] is that the relationship between changes of secondary structure and US treatment conditions was revealed. Results showed that α-helix content was generally increased with the extended duration of US treatment, but no significantly changed with the increase of US power. As explained by authors, this observation may be related to the DG, and the higher DG endowed MPI-glucose lower αhelix content with the extended US treatment. However, this statement cannot properly explain the phenomenon since DG was increased with the extended duration of US treatment. Therefore, further studies are needed to evaluate effect of US power and duration on the secondary structure of proteins. Besides the soybean, buckwheat is another important source of plant origin protein. The proteins in buckwheat have well-balanced amino acid composition with protein content about 8.51 to 18.87%. Many potential health effects of buckwheat protein include hypolipidemic activity, cholesterol-lowering effects etc. [62,63]. US was adopted to promote the MR between buckwheat protein isolate (BPI) and dextran as reported in [64], and a significantly improved emulsifying properties of the conjugates was observed compared with that treated by conventionally thermal processing. Surface activity analysis showed that the initial BPI formed loose adsorption at an oil–water interface, and each molecule occupied a large area. After the glycation with dextran, the BPI-dextran conjugates were closely packed, therefore, made each molecule occupied a small area of the interface. The BPI-dextran conjugates obtained by US, in particular, occupied a smaller area at the interface, tended to be closely packed, and formed a thicker interfacial film compared with those obtained by thermal processing. This phenomenon would be further attributed to a higher amount of dextran attached to the BPI, as well as a significant electrostatic shielding decreased the repulsion between BIP [65]. Another study focusing on the MR between peanut protein isolate (PPI) and maltodextrin was conducted at a relatively low pH value of 3.8 for producing an effective emulsifying agent for low pH application. Under the acidic condition, rate of MR would be significantly decreased compared with neutral or alkaline condition. As a consequence of low pH, DG of PPI-maltodextrin conjugates was only achieved 26.8% after a 48 h-wet-heating treatment; however, the DG would be achieved at the same level after an US-assisted wet-heating within 40 min. Either native PPI or PPI-maltodextrin conjugates obtained by wet-heating alone were unstable due to immediate bridging flocculation and coalescence of droplets. For the PPI-maltodextrin treated by US for 100 min, DG was achieved to 35.6%, and made it become more stable with a smaller mean size of droplet, as well as high solubility and surface activity.

groups on the surface of protein molecules in contact with the polar aqueous environment. US or thermal treatment could expose some of the hydrophobic groups initially buried in the interior of protein molecules to the surface and thus increase the H0 of proteins. As a result of MR between SPI and sugars, both US and thermally treated groups showed an increase of H0 compared with the native SPI [57]. However, a decrease of H0 was observed in glycated SPI through either US or thermal treatment compared with heated SPI without participation of sugars. This phenomenon indicates that the glycation had the protective effects against protein denaturation during heat treatment, reducing exposure of hydrophobic residues to the surface of the protein molecule. Furthermore, protein aggregation and formation of advanced glycation products or melanoidins would also result in a decrease of H0. Furthermore, 37.0% and 25.1% increase in H0 for SPI-glucose and SIPmaltose systems was observed with the assistant of US compared with that processed by thermal treatment, respectively. Cavitation and micro-streaming forces generated during the US processing may lead to the exposure of the hydrophobic regions, which of them were initially buried inside the molecular interior to the surface of SPI [57]. Particle size (presented as volume-mean diameter, D43) of SPI-glucose MRPs and SPI-maltose MRPs was remarkably decreased by 22.7% and 5.1% after the US treatment, respectively. This phenomenon is mainly caused by the dissociation of macromolecular protein and disruption of noncovalent bonds between SPI molecules when treated by US [45]. Rheological properties were presented by change in storage modulus (G’) of both SPI-glucose and SPI-maltose conjugates during acidification. Results show that significantly higher G’ for the both MRPs prepared by US was determined compared with those processed without US. The exposed hydrophobic regions from the interior to the surface of SPI, and the relatively small particle size of MRPs would contribute to an easier formation of an acid-induced gel network by hydrophobic interaction of SPI. Another similar study on US-MR between SPI and gum acacia was conducted [58]. Besides similar findings, emulsifying properties, including emulsifying activity and stability index were determined. Gum acacia is confirmed to have an excellent emulsifying capacity and emulsion stabilizing properties that would lower the interfacial tension at a hexadecane-water interface [59]. After combining gum acacia with SPI, SPI-gum acacia conjugate obtained by US gave emulsions more stability against creaming than the native SPI and the control obtained by conventional heat treatment without US. Besides the important role of gum acacia, changes in SPI conformation and structure by the US treatment were also attributed to the improved emulsifying properties. Jambrak, Lelas, Mason, Krešić and Badanjak [60] focused on studying SPI exhibited partial unfolding of 7S and 11S fractions and an aggregation of proteins (especially 11S fraction) after the US processing. Partial denaturation and a more disordered structure are capable of providing a better potential for adsorption at the oil–water interface. A further analysis on lysine and arginine content after the glycation was proved that the two amino acids residues attended the covalent linkage between the SPI and gum acacia. Analysis on secondary structure of SPI-gum acacia conjugate obtained by US treatment indicated that the grafted conjugation had decreased α-helix and β-sheet levels and increased random coli level. Since the structures and functions of conjugations are highly correlated, the promoted attachment of gum acacia to SPI led to changes in spatial structure and unfolding of protein molecules, therefore, decreased α-helix and β-sheet of proteins which were normally buried in the interior site of SPI. On the contrary, the increased random coli level was attributed to unfolding of proteins and breaking of peptide bonds after the US treatment, hence, improved emulsifying properties. US treatment was also reported to improve wet-heating MR between MPI and glucose [61], as well as soy β-conglycinin and maltodextrin [51]. Similar findings on the improved DG, solubility, emulsification activity and stability, and surface hydrophobicity of the two conjugates obtained by US treatment were reported compared with those without

5.2. Ultrasound-assisted Maillard reaction for modifying animal origin proteins/peptides Whey protein is considered as a high-quality protein source because of widely available, easily digested and absorbed. Whey protein isolate (WPI) is a by-product of cheese whey industry with high nutritional value and functional properties [66]. However, functionalities of WPI are sensitive to pH, ionic strength and temperature, which restrict its wider application in diverse food systems. Glycation of WPI with gum acacia was first conducted with/without US treatment [67]. Compared with the conventional wet-heating, covalent linkage of WPI with gum acacia through MR was significantly promoted by US, and DG of WPIgum acacia was reached to 26.23% with an 80 min-US treatment. Significantly lower browning intensity, and promoted solubility under alkaline condition, thermal stability and emulsifying properties were observed for the WPI-gum acacia obtained by US. Another study developed WPI-galactose and whey protein peptide (WPP)-galactose conjugates through US-MR [68]. Promoted antioxidant capacities of two conjugates obtained by a 60 min-US treatment were emphasized. The higher antioxidant capacity of WPP-galactose is an indicator for a better function of WPP-galactose than the WPI-galactose conjugate. Different from the previous two studies, whey proteins (WP) were 8

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first reported to be glycated by arabinose under macromolecular crowding conditions with polyethylene glycol with a molecular weight of 6000 (PEG 6000) as crowding agent [26]. Compared with thermal one, an increase in efficiency of glycation and only slight changes of WP structure was observed in US-MR. The macromolecular crowding intensities oxidative modification of WP and formation of amyloid-like structures. Solubility, thermal stability and antioxidant capacity of WParabinose conjugate were enhanced compared with the native WP. Therefore, US treatment under crowding conditions would enhance the glycation, enable short processing time and mild conditions, while preserve basic structure of WP and minimize its aggregation. Similar findings were reported in a glycation of β-Lactoglobulin (BLG) as a major constituent of WP with 6 different reducing sugars. Among the reducing sugars, ribose as one of the most reactive reducing sugar inducted the highest DG of BLG (76%) with assistant of US [69]. This result is accordance with the evaluation of reactivity of reducing sugars which was decreased in the following order: aldopentoses > aldohexoses > aldoketoses > disaccharides > polysaccharides [70]. Ovalbumin (OVA) is one of proteins produced from egg white. Utilization of OVA is very limited during food processing since changes in the functional properties of OVA are easily happened. Significantly improved foaming properties, physicochemical and structural characteristics of OVA were observed after US-assisted glycation with xylose. Some minor changes on the subunits and secondary structure of OVA indicated that the tertiary structure was slightly changed and became more flexible and loose after the US-assisted glycation [71]. A similar study on US-assisted glycation of bovine serum albumin (BSA)glucose showed that secondary structure of BSA was significantly changed after US treatment compared with the thermal one, including a decreased percentage of α-helix and β-turns, as well as an increased percentage of β-sheet and random coli. A further investigation on different intensity of US on the changes of secondary structure of BSA indicated that very limited influence on the secondary structure of BSAglucose conjugates with US intensity ranging from 10.19 to 17.83 W/ cm2. Results indicated very limited impact of US intensity on the secondary structure of protein in the certain range [72]. Besides glycation of proteins, Abdelhedi, Mora, Jemil, Jridi, Toldrá, Nasri and Nasri [73] chose peptides obtained from smooth hound viscera protein hydrolysates (SHVPH) as research subjects, and further glycated with sucrose to from conjugates with promoted functions. Fish viscera represent a huge part of the discards rejected in the fish industry and fish markets; therefore, it is worthy to properly adopt emerging technologies to produce final products with improved physical, chemical, and sensory properties of SHVPH-sucrose conjugates. With an assistance of US pre-treatment, DG of SHVPH-sucrose conjugates was significantly increased, especially the SHVPH obtained by esperase. Moreover, bitter taste was potentially reduced for the SHVPH-sucrose conjugates obtained by US since free amino acid residues responsible to the bitter taste were reduced by up to 54.55% after the US-assisted glycation. The reduction in bitter attribute of SHVPH is an important criterion in food formulations. A similar study was conducted by [74], which reported an enhanced MR between mussel meat protein hydrolysate (MMPH) and glucose/xylose with assistant of US. Results of GCMS and amino acid analysis show that the final sample processed by US was rich in meaty and seafood flavors but lower bitterness compared with thermally treated sample. Antioxidant capacity, including DPPH radical scavenging activity and reducing power of the sample obtained by US-MR was about 5%-20% higher than those obtained by thermal one. As summarized in both studies, US-MR would become a potential strategy to prepare meaty flavors from different animal origins. Possible mechanism of US-MR between protein and saccharide is shown in Fig. 3. Unfolding of protein and braking of peptide bonds are first hydrolyzed by the extremely high temperature and pressure generated by US. The collision is increased between the reactive groups, and subsequently speeds up the conjugation processing through the US treatment. The conventional wet-heating normally requires a higher

processing temperature and longer duration in order to obtain the glycated proteins with the same DG compared with US-assisted glycation. As a benefit of US, a significantly shorter time with a lower level of browning using US is achieved at the same DG compared with the conventional wet-heating without US [51]. 6. Application of ultrasound in food processing involving Maillard reaction For now, US is still a relatively new technology in food processing, which has been gradually developed as a promising mean of homogenization, extraction, cutting, inactivation of microorganisms and enzymes, drying enhancement, etc. In this section, applications of US in food systems with any changes of attributes involving MR were to be reviewed. Both promoted and inhibited attributes brought by US are summarized in Table 3. 6.1. Ultrasound-assisted Maillard reaction in liquid and semi-liquid foods processing Honey is a supersaturated solution of glucose, which tends to crystallize at room temperature in the form of glucose monohydrate. The crystallization in honey makes it hard to be processed in the food industry due to thickness and high viscosity [75]. For retarding the crystallization in Turkish honeys, Önür, Misra, Barba, Putnik, Lorenzo, Gökmen and Alpas [76] adopted US (frequency: 24 kHz, power: 400 W) as a replacement of conventionally thermal treatment (60 °C, 2 h). Results showed that the honeys underwent US processing have achieved the same liquefaction of honeys. As a negative aspect brought by thermal treatment, toxic 5-hydroxymethylfurfural (HMF) would be generated through MR as a final MRPs; however, 61.9%, 82.6%, and 80.9% decrease in HMF content was detected after the US processing compared with those in thermal one in canola, cotton, and sunflower honey, respectively. HMF can be formed through both MR and caramelization. The degradation of Amadori compounds is able to form the HMF in the intermediate stage of MR if sufficiently high energy is provided. To generate HMF through the caramelization, however, normally requires higher temperature than the MR, and an acidic condition is preferred for sugar fragmentation. Another negative aspect brought by MR was generation of browning color. Similarly, more than 2.2 times decrease in L* value was observed in the US-processed honeys compared with those after thermal processing. Therefore, US as a processing intervention for honey is advantageous over thermal treatment since less generation of HMF and colored MRPs. Another study has evaluated impact of US on longan, lychee and wildflower honeys collected from Northern Thailand [77]. The conventionally thermal treatment was conducted at 90 °C for 5 min whereas US processing (frequency: 20 kHz, power: 130 W) was sufficiently high to eliminate microbes reaching to the complied limits of the Thai Agricultural Standard (TAS 8003–2013). Moreover, 31.1%, 36.5%, and 50.4% less of HMF content was detected compared with those processed by thermal treatment in longan, lychee and wildflower honey, respectively. Browning index of US-processed honeys was also significantly lower than those undergoing thermal processing. Analysis of honeys color showed that the honeys processed by US inhibited formation of reddish and yellowish color. Changes of temperature in honeys during US treatment were determined to be 52.63 °C and 75.09 °C with amplitude of 40% and 80%, respectively. Therefore, it is possible that the lower content of colored MRPs generated during US processing would be attributed to relatively lower temperatures compared with 90 °C used in thermal processing. Another positive aspect brought by US is increased content of total phenols and flavonoids in the US-processed honeys due to US stimulation as a mean of disintegration of pollen and promoted extraction of functional compounds [78,79]. Thermal treatment at the high temperature would partially destroy phenols and flavonoids because of thermal degradation and non-enzymatic auto9

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Fig. 3. Schematic of US-MR between protein and saccharide based on [51]; [S] refers to oxidation products of mercapto group.

globule membranes were severely damaged, and the protein structure underwent a considerable change. Moreover, the promoted interaction would lead to the coalescence of particles, and change in the whipped cream network structure. Therefore, air bubbles became close to each other and decreased stability of whipped cream. The colored MRPs generated by US-MR gave significant impact on overall color of whipped cream. Compared with the thermally treated whipped cream, yellowness parameter (b value) was increased with the increase of US power. A further sensory evaluation was conducted, and the lowest score on color but the highest score on organoleptic properties of USprocessed whipped cream were given. The highest score on organoleptic properties was mainly attributed to the decreased particle size and less coalescence of fat cells resulting in a smooth mouthfeel in the texture. No further analysis on flavor composition may suggest very limited change on overall flavor profile of whipped cream after the US treatment.

oxidation. As concluded in this study, US with low amplification would become an alternative preservation technology for maintaining the high quality of honeys. US-assisted processing is also an alternative technology in dairy industry. Engin and Karagul Yuceer [80] adopted an US treatment targeting inactivation of microbes in milk. However, US processing (frequency: 20 kHz, power: 500 W) was insufficiently high to reduce the number of bacteria, yeasts and molds in milk, such as Escherichia coli and Staphylococcus spp. Besides the poor inactivation of microorganisms, some off-flavors as MRPs were also detected in the US processed samples but absent in the thermal one. For example, methional as a sulfur-containing volatile compound presented a meaty-like and powerful onion odor, which would be attributed to an off-flavoring impact in the US-processed milk [81,82]. Moreover, a significantly higher concentration of organic acids was formed in the US treated-milk sample through promoted lipid oxidation, including butyric acid, pentanoic acid, and hexanoic acid. Meanwhile, other volatile compounds, e.g. hexanal, 1-dexen-3-one, maltol, 2-nonenal, etc. were possibly generated through the US-MR. As concluded in this study, the US treatment was not effective enough in reducing certain groups of microorganisms, and some unique volatile compounds generated during US treatment may not be favored by milk product as well. Another application of US on liquid food is a typical Chinese large beer [83]. The beer was treated by US (frequency: 24 kHz, volumetric power: 2.7 W/mL) for 2 min at different temperature levels ranging from 40 to 60 °C. The US-treated beer at 40 °C was insufficiently high enough to inactivate yeasts, lactic acid bacteria and aerobic bacteria; when temperature was raised to 50 or 60 °C with US treatment, both yeast and bacteria became undetectable. Other quality attributes of UStreated beer largely remained unchanged compared with the heat pasteurized beer. However, a significant increase of browning color at 60 °C with US treatment was observed, which is attributed to the promoted generation of colored MRPs. Three staling compounds were determined, including trans-2-nonenal, furfural, and 3-methyl butanal. Among these, both furfural and 3-methyl butanal were generated through the MR, which are indicators of heat-induced flavor damage and beer oxidation. Therefore, a significantly high content of furfural and 3-methyl butanal was formed after US treatment at 60 °C due to the promoted MR and oxidation of beer, and these salting compounds would bring negative impacts on overall flavor of aged beer. As concluded in this study, US-assisted thermal treatment has great potential on beer processing; however, thermal effect brought by US should be carefully evaluated; otherwise off-flavors, unfavored color, and microbial residue would become big issues if temperature was too high or too low. Different from liquid foods, US is applicable to process semi-liquid foods as well. Amiri, Mousakhani-Ganjeh, Torbati, Ghaffarinejhad and Kenari [84] applied an US treatment (frequency: 20 kHz, power: 100–300 W) to process whipped cream at 50 °C with treatment duration ranging from 5 to 15 min. After the US treatment with low power, the interactions on the surface of fat cells with milk protein in the whipped cream were promoted the formation of a network around the air bubbles. Such a network would prevent the migration of air bubbles, and subsequently increase the stability of the whipped cream structure [85,86]. However, if the input power of US was raised to 300 W, the fat

6.2. Ultrasound-assisted Maillard reaction in drying of foods Airborne US is an emerging technology for drying foods, especially vegetables and fruits. Airborne US is a cyclic sound wave that is transferred away from the emitter across air media. After combing with convective drying, mechanical effects brought by US can reduce internal and external mass transfer resistance without generating high level of thermal energy during convective drying. Microstreaming, oscillating velocities, and pressure variations are introduced at gas–solid interfaces; meanwhile, rapid alternation between expansion and compression cycles on the internal structure can trigger a faster evaporation rate of moisture, as well as increase mass transfer and diffusion. Frias, Peñas, Ullate and Vidal-Valverde [87] adopted an airborne US-assisted convective drying and observed a higher retention of vitamin C and βcarotene compared with the control without the assistance of US. Color change of green pepper showed that ΔE values were determined to be 11.32 and 11.51 after US-assisted convective drying with power of 100 W and 200 W, respectively, which were significantly lower than that obtained by convective drying at 54 °C with ΔE value of 15.12 [88]. A similar US-assisted convective dried apple slices reduced the total color change by about 32% at power of 200 W in comparison with the convective drying [89]. Therefore, a significantly lower temperature level would be required to completely dry target foods without compromising their quality since heat-sensitive compounds would be largely preserved during the US-assisted drying. Besides the preservation of heat-sensitive compounds, MR is also inhibited during US-assisted drying due to a lower temperature compared with the convective drying. Detailed elucidations of airborne US-assisted convective drying can be found in a comprehensive review prepared by Fan, Zhang and Mujumdar [90]. Pre-treatment of target foods through US before drying is another strategy widely adopted in the food industry. Nonuniform temperature distribution during drying would raise a big problem and influence on quality of dried food products. As one of significant benefit brought by the US pre-treatment, fewer hot spots were spotted in the target foods if pre-treated by US compared with untreated or hot-water treated target foods during drying processing. This phenomenon is possibly attributed to the enhanced water output from micro-channels during US-assisted 10

11

20 kHz, 500 W 24 kHz, 2.7 W/mL, 350 W/cm2, 40–60 °C, 2 min

20 kHz, 100–300 W, 50 °C, 5–15 min

Milk Chinese large beer

Whipped cream (30% fat content) Apples

2

1

25 kHz, 1 W/cm US-assisted osmotic drying with fructose or d-sorbitol (40%), 35 °C, 120 min 20 kHz, 1200 W, 30–90% amplitude USassisted intermediate-wave infrared drying (60 °C, 1.5 m/s) 60 °C, 10 min, US blanching-assisted convective drying (46 °C, 4.9 m/s) 95 °C, 5 min, blanching without US

Intermediate-wave infrared drying without US pretreatment

Osmotic drying without US pretreatment

85 °C, 10 min, thermal processing

Decreased terpene and ester content synthesized through MR ↓92.7% of 2-FM-Lys and 2-FM-Arg content;↓ 13%-44% of drying time

–

[92,93]

[91]

[89]

–

[80] [83]

[84]

Brighter and less brown color of dried carrot

Content of acidic compounds was increased; increased color, protein sensitivity, colloidal haze;increased salting compounds as negative flavors, including furfural, 3methyl butanal, and trans-2-nonenal Uniformed distribution of particle diameter; increased foam stability; increased yellowness Increased a* value meaning that color shifts tored shades

[77]

[76]

Refs.

–

Enhanced browning index and reddish and yellowish color;

90 °C, 5 min, thermal processing

65 °C, 30 min, thermal processing Pasteurization

↓75.4% of HMF content 2;↓224.8% of L* value ↓31.1%, ↓36.5%, and ↓50.4% of HMF content for longan, lychee and wildflower honey, respectively – –

–

60 °C, 2 h, thermal processing

1

Inhibited attributes

Attributes compared with the control Promoted attributes

Control group

“–” refers to not reported in this study. “↓” refers to the attribute significantly inhibited in the target food processed by US compared with that processed by conventional treatment without US.

Carrots, strawberries

Carrots

24 kHz, 400 W, 20%-100% amplitude, 50 °C, 106 min 20 kHz, 130 W, 40% (52.63 °C) and 80% (75.09 °C) amplitude, 30 min

Sunflower, cotton, and canola honey Longan, lychee and wildflower honey

2

US conditions

Target foods

Table 3 Summary of promoted/inhibited attributes related to MR in the foods obtained by US-assisted food processing.

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through the lipid oxidation, many of them are unable to transfer into the water phase where a number of desired flavors are generated through the MR. It is easy to separate the oil and water phases through the centrifugation. Moreover, degassing effect brought by US is fatal for expulsion of flavors generated through MR. The developed CUTR and CUPS may provide a better solution for largely keeping food flavors in a relatively closed system for US processing. In conclusion of studies on MR model systems, US plays an important role on promoting the intermediate stage and final stages of MR. The generation of colored and volatile MRPs, as well as MRPs with higher antioxidant capacity are promoted by the US. The enhanced flavor generation in both simple MR model systems and oil-in-water MR model systems provides alternative strategies to produce higher concentration and more food flavors through the US-MR. Both plant or animal origin proteins have high nutrition and various functions. It is necessary to further improve functional properties of the proteins to extent their utilization in the food industry. Among methods for modification of protein, reaction of proteins with saccharides is one of promising ways without adding external chemicals [51,68]. Reactive amino sites (e.g. arginine- or lysine-end) are normally hided inside the protein, which makes the rate of MR between protein and saccharide become extremely low. Therefore, US is adopted to provide an environment of extremely high, albeit momentary temperature and pressure, and further accelerates steps of unfolding protein and braking peptide bonds. The collision is simultaneously increased between the reactive groups on protein surface and saccharides, therefore, speeds up the conjugation processing through the US treatment. A significantly shorter time of MR with a lower level of browning of glycated proteins is achieved by using US, and the same DG of protein can be achieved compared with the thermal treatment without US. Further investigation on changes of secondary structure of US-treated proteins shows a decrease of α-helix and β-turns, as well as an increase of β-sheet and random coli of glycated protein. Besides the higher DG of US treatedprotein, promoted functional properties of glycated proteins obtained by US are extensively reported, including enhanced solubility, emulsifying stability and activity, surface hydrophobicity, foaming ability, antioxidant capacities, etc., as well as decreased particle size, bitterness taste, etc. In conclusion, the US-MR between proteins and saccharides is a promising way to significantly decrease reaction time and increase DG of protein. It is also capable of promoting functional activities of glycated proteins, which make them extensively used in the food industry. So far, US has been adopted as an alternative technology for food processing. One significance of US is capable of partially taking replace of conventionally thermal treatment, therefore, leading to a decrease of processing time and temperature. As a results of decreasing treatment duration, higher content of nutrients and functional ingredients would be preserved in the US processed-foods. The MR during US treatment is inhibited to a certain level as well, which prevents loss of essential components in the final products. Application of airborne US on convective drying is a good example, which achieves the decrease of drying time and temperature, and the increase of drying efficiency. As results of the inhibited MR, less content of colored MRPs, off-flavors (e.g. furfural, 3-methyl butanal, etc.), and AGEs as hazard MRPs (e.g. HMF, 2-FM-Lys, 2-FM-Arg, etc.) are formed in the processed food with assistance of US. Moreover, contents of vitamin C and β-carotene in carrots were largely preserved in the US-dried product. Other applications of US are expected to promote the MR. Antioxidant capacity, organoleptic properties (e.g. desirable browning color, more flavors, etc.), and functional properties (e.g. foam stability, emulsion stability, etc.) of final products are enhanced by the US-MR. We should aware that the US-MR is a double-edge sward for the final products. As discussed previously, acrylamide, HMF, furans, heterocyclic amines, and other AGEs are very likely to be formed simultaneously through the US-MR. Although very limited studies concerned these hazards formed in the US-MR for now, safety assessment of

pre-treatment. Therefore, the drying time for samples pre-treated by US was significantly decreased with the evenly distribution of heat during subsequently time. Wang, Xu, Wei and Zeng [91] applied an US pretreatment (frequency: 20 kHz, power: 1200 W, amplitude: 30–90%) to carrot slides followed by an intermediate-wave infrared radiation drying (60 °C, 1.5 m/s). Results show that β-carotene as a functional compound in carrots was largely preserved after the US pre-treated drying, which was 32.1% of β-carotene content higher than that without the US pre-treatment. Color change during drying process are determined by various factors, including change of original colored compounds, such as carotenoids through oxidation, and generation of more colored compounds through enzymatic or nonenzymatic browning. The dried carrot with US pre-treatment had a lower ΔE value and lighter browning color compared with the one without US pretreatment, and the lower ΔE value in the US pre-treated carrot samples indicated a closer color compared to the raw carrot. A further investigation on aroma of dried carrots through electronic nose showed that a decrease of terpene and ester biosynthesized through MR was again proved the inhibition of MR during US pre-treated drying. Another similar study focused on drying carrots and strawberries after an US-assisted blanching [92]. The US-assisted blanching was conducted at either 60 °C with 10 min for minced carrot, and 70 °C with 15 min for sliced carrot. Temperatures of both US-assisted blanching were lower than the hot water blanching at 95 °C for 5 min. Results show that 13% to 44% of drying time was saved with the US-assisted blanching of target foods compared with hot water blanching without US. As a result of lower blanching temperature and drying time, MR was extensively inhibited during blanching-drying, and 140.8% less of 2-FM-Lys and 2furoylmethyl-arginine (2-FM-Arg) content was quantified in the dehydrated carrot sample processed with US-assisted blanching. This result is accordance with Villamiel, Gamboa, Soria, Riera, García-Pérez and Montilla [93], which observed a 92.7% less of 2-FM-Lys and 2-FM-Arg content in the dried carrot with US-assisted blanching. As concluded in these studies, US pre-treatment of target foods has brought many positive aspects to subsequent drying procedure, including enhancement of drying performance, reduction of duration and/or temperature required by drying, and better preservation of the microstructure of dried foods. MR occurred during drying, therefore, is partially inhibited with reduced generation of unfavored colored and volatile MRPs in the dried foods. 7. Discussion and conclusions Fundamental studies on US-MR model systems are first observed a promoted depletion of reactants, as well as generation of intermediate MRP and final MRPs with color and flavor. Furthermore, kinetic studies on US-MR model systems have provided more insights into sub-steps of MR which are promoted or inhibited by US. In general, formation of dicarbonyl compounds as intermediate stage of MR is significantly promoted by US. As a result of high content of dicarbonyl compounds as precursors of final MRPs, higher concentration of many MRPs generated in the final stage are detected simultaneously, including melanoidins, organic acids, and pyrazines. Other step for forming flavor compounds, e.g. aldol-type condensation as a pressure-favored reaction, is promoted mainly due to a high-pressure environment generated by US. Through the aldol-type condensation, a number of unique volatile MRPs are only generated in the US-MR but absent in the thermal counterpart. Isomerization of reducing sugars (e.g. glucose is isomerized to fructose) is inhibited since the isomerization is a competing reaction against MR. Further investigations on the oil-in-water MR model systems show an even better enhancement on flavor generation brought by US. Lipid oxidation is accelerated, and more carbonyl compounds as oxidation products of oils are generated with the assistance of US. The carbonyl compounds are water-soluble, and subsequently impart into the MR as intermediates, therefore, promote the MR which is normally occurred in the water phase. Although off-flavors are generated simultaneously 12

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final products is strongly recommended when the MR is extensively involved. Besides the harmful MRPs, off-flavors, undesirable colors, loss of nutrients may also happen due to the US-MR. Therefore, it is necessary to adopt the proper US processing conditions for balancing both positive and negative aspects brought by the US-MR.

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8. Recommendations for future aspects US-MR is a new topic in the food science domain. It provides an alternative mean of promoted generation of food flavors, enhanced modification of food proteins, and improved quality of food products. Based on our experiences, the following recommendations for future aspects are given. First of all, it is worthy to further explore effects of US on MR through kinetic study. Although some of MR steps have been proved to be promoted/inhibited by US, there are still uncertainties since complexity of MR mechanisms. One example is inhibited generation of acrylamide as a carcinogenic MRP throughout US-MR; however, no further elucidation on reaction mechanisms was given [15]. Therefore, we suggest that reporting promoted/inhibited MRPs in the US-MR is not enough at this stage, but more mechanisms should be given according. Secondly, promoted flavor generation is one of key attributes brought by US-MR. For now, only the aldol-type condensation as a critical step for forming complex pyrazines was reported in [9]. Since a number of unique pyrazines, esters, and aldehydes were only generated in US-MR, it is worthy to further elucidate reaction mechanisms and propose potential ways to enhance flavor generation. In addition, negative aspects brought by US-MR should be carefully evaluated when apply US to achieve the glycation of proteins. A further study is necessary to isolate the glycated proteins from the model systems at the end of protein glycation, and separate hazard components generated in the US-MR model systems. Lastly, mathematic modelling is a powerful tool for revealing relationship between US conditions and changes of attributes related to MR. An example is utilization of quantitative modelling approaches to optimize US conditions for nonenzymatic browning and ascorbic acid degradation in orange juice [94]. It is recommended to further dig out relationship between US and attributes related to MR for identifying optimal processing regions and eliminating quality deterioration of target foods. Declaration of Competing Interests The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements The following founding sources are gratefully acknowledged: National Key R&D Program of China (2018YFC1602300), China Postdoctoral Science Foundation funded project (2018M642165), the Fundamental Research Funds for the Central Universities (JUSRP11904), the Natural Science Foundation of Jiangsu Province (BK20171139). I, Dr. Hang Yu, also wants to thank my wife who brought my beloved daughter, Wenqi Yu to our life. References [1] H. Lee, H. Feng, Effect of power ultrasound on food quality, in: H. Feng, G. BarbosaCanovas, J. Weiss (Eds.), Ultrasound Technologies for Food and Bioprocessing, Springer, New York, New York, NY, 2011, pp. 559–582. [2] L. Chen, J. Chen, K. Wu, L. Yu, Improved low pH emulsification properties of glycated peanut protein isolate by ultrasound Maillard reaction, J. Agric. Food Chem. 64 (2016) 5531–5538. [3] D. Zhu, S. Damodaran, J.A. Lucey, Physicochemical and emulsifying properties of whey protein isolate (WPI)−dextran conjugates produced in aqueous solution, J. Agric. Food Chem. 58 (2010) 2988–2994. [4] Y. Liu, G. Zhao, M. Zhao, J. Ren, B. Yang, Improvement of functional properties of peanut protein isolate by conjugation with dextran through Maillard reaction, Food

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