Decontamination by ultrasound application in fresh...

15
Review Decontamination by ultrasound application in fresh fruits and vegetables Jackline Freitas Brilhante de São José a , Nélio José de Andrade b, * , Afonso Mota Ramos b , Maria Cristina Dantas Vanetti c , Paulo César Stringheta b , José Benício Paes Chaves b a Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil b Food Technology Department, Federal of Viçosa University, 36570-000 Viçosa, Minas Gerais, Brazil c Microbiology Department, Federal of Viçosa University, Viçosa, Minas Gerais, Brazil article info Article history: Received 18 November 2013 Received in revised form 7 April 2014 Accepted 9 April 2014 Available online 19 April 2014 Keywords: Ultrasound Fruits Vegetables Food quality abstract Changes in consumer eating habits, health concerns, and convenient and practical foods have led to an increased demand for fruit and vegetable products. Food safety is essential considering that there are reports of outbreaks involving the consumption of fruits and vegetables contaminated with pathogens. Washing associated with sanitizer procedure is considered as a critical step to satisfy hygienic and sanitary requirements and maintain the sensory and nutritional characteristics of fruits and vegetables. Chemical compounds are widely applied to clean and sanitize fresh fruits and vegetables, and some of these chemicals, such as the inorganic chlorine compounds, produce by-products that are dangerous to human health. The use of ultrasound is a technology that is gaining ground in the food industry. Ul- trasound is a form of energy generated by sound waves at frequencies that are too high to be detected by the human ear. In ultrasound, the removal of dirt and food residues from surfaces and the inactivation of microorganisms occur as a consequence of cavitation, which is the formation, growth and collapse of bubbles that generate a localized mechanical and chemical energy. There are indications that this technology can be used in the food industry, alone or associated with chemical sanitizers. In this paper, we discuss the principles, mechanisms and effects of ultrasound on fruits and vegetables as a sanitization technology. Ó 2014 Elsevier Ltd. All rights reserved. Contents 1. Introduction ....................................................................................................................... 37 2. History of ultrasound ............................................................................................................... 37 3. Principles of ultrasound ............................................................................................................. 37 3.1. Generation of power ultrasound .................................................... ............................................ 40 3.2. Available equipment ......................................................... ................................................. 40 3.3. Factors affect ultrasound application in fresh fruit and vegetables ................................................................... 40 4. Microbial inactivation ............................................................................................................... 41 5. Effect of ultrasound on the properties of fruits and vegetables ........................................ .................................. 44 5.1. Inactivation of enzymes ........................................................................................................ 44 5.2. Effect on food components ..................................................................................................... 45 5.3. Sensory aspects .............................................................................................................. 46 6. Consumer acceptance ............................................................................................................... 47 7. Industrial uptake, status update and challenges faced by the food industry .................................. ............................. 47 8. Conclusion ........................................................................................................................ 47 * Corresponding author. Tel.: þ55 31 3899 1855. E-mail addresses: [email protected] (J.F.B. São José), [email protected] (N.J. Andrade). Contents lists available at ScienceDirect Food Control journal homepage: www.elsevier.com/locate/foodcont http://dx.doi.org/10.1016/j.foodcont.2014.04.015 0956-7135/Ó 2014 Elsevier Ltd. All rights reserved. Food Control 45 (2014) 36e50

Transcript of Decontamination by ultrasound application in fresh...

lable at ScienceDirect

Food Control 45 (2014) 36e50

Contents lists avai

Food Control

journal homepage: www.elsevier .com/locate/ foodcont

Review

Decontamination by ultrasound application in fresh fruits andvegetables

Jackline Freitas Brilhante de São José a, Nélio José de Andrade b,*, Afonso Mota Ramos b,Maria Cristina Dantas Vanetti c, Paulo César Stringheta b, José Benício Paes Chaves b

a Federal University of Espírito Santo, Vitória, Espírito Santo, Brazilb Food Technology Department, Federal of Viçosa University, 36570-000 Viçosa, Minas Gerais, BrazilcMicrobiology Department, Federal of Viçosa University, Viçosa, Minas Gerais, Brazil

a r t i c l e i n f o

Article history:Received 18 November 2013Received in revised form7 April 2014Accepted 9 April 2014Available online 19 April 2014

Keywords:UltrasoundFruitsVegetablesFood quality

* Corresponding author. Tel.: þ55 31 3899 1855.E-mail addresses: [email protected] (J.F.B. São J

http://dx.doi.org/10.1016/j.foodcont.2014.04.0150956-7135/� 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

Changes in consumer eating habits, health concerns, and convenient and practical foods have led to anincreased demand for fruit and vegetable products. Food safety is essential considering that there arereports of outbreaks involving the consumption of fruits and vegetables contaminated with pathogens.Washing associated with sanitizer procedure is considered as a critical step to satisfy hygienic andsanitary requirements and maintain the sensory and nutritional characteristics of fruits and vegetables.Chemical compounds are widely applied to clean and sanitize fresh fruits and vegetables, and some ofthese chemicals, such as the inorganic chlorine compounds, produce by-products that are dangerous tohuman health. The use of ultrasound is a technology that is gaining ground in the food industry. Ul-trasound is a form of energy generated by sound waves at frequencies that are too high to be detected bythe human ear. In ultrasound, the removal of dirt and food residues from surfaces and the inactivation ofmicroorganisms occur as a consequence of cavitation, which is the formation, growth and collapse ofbubbles that generate a localized mechanical and chemical energy. There are indications that thistechnology can be used in the food industry, alone or associated with chemical sanitizers. In this paper,we discuss the principles, mechanisms and effects of ultrasound on fruits and vegetables as a sanitizationtechnology.

� 2014 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 372. History of ultrasound . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 373. Principles of ultrasound . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

3.1. Generation of power ultrasound . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403.2. Available equipment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403.3. Factors affect ultrasound application in fresh fruit and vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40

4. Microbial inactivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415. Effect of ultrasound on the properties of fruits and vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44

5.1. Inactivation of enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445.2. Effect on food components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 455.3. Sensory aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46

6. Consumer acceptance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477. Industrial uptake, status update and challenges faced by the food industry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47

osé), [email protected] (N.J. Andrade).

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 37

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47

1. Introduction

The increased consumption of fruits and vegetables has led to anincreased concern about the high quality of nutritional, sensory andmicrobiological aspects of these foods (Chemat, Zill-e-huma, &Khan, 2011; Fava et al., 2011; Martinéz-Sánchez, Allende, Bennett,Ferreres, & Gil, 2006; Plaza et al., 2011; Vandekinderen et al., 2009).Safety and quality are important terms in the food industry.Recently, there has been great interest in new methods to ensurethe preservation of food without the use of additives and mainte-nance of the food’s nutritional value and sensory aspects with low-energy consumption, at a competitive cost, and using environment-friendly products with a high degree of safety.

To minimize the risk of microbial contamination, potentialsources should be identified, and specific preventive measuresshould be implemented.

To prepare ready-to-eat fruits and vegetables, the produce mustbe clean, safe, and free of soil residue, insects, metals and weeds.Fruits and vegetables should be carefully cleaned before processingbecause fresh-cut produce is processed from material grown incontact with soil and without any antimicrobial treatments.

The inclusion of a washing and sanitization steps before cuttingand during processing effectively reduces the risk of pathogen andresidue contamination on fruits and vegetables from harvest andhandling conditions. During sanitization, fruits and vegetables aresubjected to an effective treatment to destroy or reduce the numberof pathogenic microorganisms, without affecting the quality, safetyor product. The effectiveness of washing to remove soil impuritiesand microbial contaminations is related to numerous factors, suchas raw material spoilage, the duration of washing, the water tem-perature, the method of washing (dipping, rinsing, or dipping/blowing), the type and concentration of the sanitizer and the typeof fresh-cut fruit or vegetable. The selection of a sanitizer for freshfruits and vegetables that are consumed raw is important, and thusthe selected product should not only be effective in the eliminationof pathogenic microorganisms but it should also be safe from atoxicological point of view.

Currently, commercial operations use wash treatments withantimicrobials as the only step to reduce microbial populations onfresh fruits and vegetables. Sanitizing with chemical solutions,which might include chlorine, primarily influences the safety andpreservation of these products (Allende, Selma, López-Gálvez,Villaescusa, & Gil, 2008; Artés & Allende, 2005; Pérez-Gregorio,González-Barreiro, Rial-Otero, & Simal-Gándara, 2011; Ruíz-Cruz,Félix, Diáz-Cinco, Islas-Osuna, & González-Aguilar, 2007; Vande-kinderen et al., 2009).

However, chlorine-based compounds are corrosive and causeskin and respiratory tract irritations to food handlers (Alvaro et al.,2009; Fava et al., 2011; Pérez-Gregorio et al., 2011; Vandekinderenet al., 2009). Water hyperchlorination generates high concentra-tions of trihalomethanes (trichloromethane, bromodichloro-methane, dibromochloromethane, tribromomethane andchloroform) and other disinfectant by-products that are potentiallycarcinogenic (Fava et al., 2011; Rico, Martín-Diana, Barat, & Barry-Ryan, 2007; Ruiz-Cruz, Felix, et al., 2007; Selma, Ibáñez, Allende,Cantwell, & Suslow, 2008; Pérez-Gregorio et al., 2011; Vande-kinderen et al., 2009). Chlorinated compounds have been the focusof environmental concerns, and some environmental groups have

suggested terminating the use of these products worldwide. InEuropean countries, such as the Netherlands, Sweden, Germanyand Belgium, the use of chlorine on minimally processed vegetableproducts is prohibited (Pérez-Gregorio et al., 2011; Rico et al.,2007). There have also been studies on emerging pathogens thatcan be more tolerant to chlorinated compounds, which raisesfurther concerns about the effectiveness and use of chlorine in theminimally processed food industry (Allende et al., 2008; Alvaroet al., 2009).

In recent years, emerging technologies, such as high pressure,pulsed electric field, electrolysed water, irradiation, ozone and ul-trasound treatments, have been widely studied for application infood industry. Studies evaluating the application of ultrasound infood science and technology have been expanded due to itspromising effects in food processing and preservation (Adekunte,Tiwari, Cullen, et al., 2010; Adekunte, Tiwari, Scannell, Cullen, &O’Donnell, 2010; Arzeni et al., 2012; Birmpa, Sfika, & Vantakaris,2013; Cameron, McMaster, & Britz, 2008; Cao et al. 2010; Chemat& Hoarau, 2004; Fava et al., 2011; Gabriel, 2012; Knorr, Zenker,Heinz, & Lee, 2004; Mothibe, Zhang, Nsor-Atindana, & Wang,2011; Nascimento et al. 2008; Patil, Bourke, Kelly, Frías, & Cullen,2009; São José & Vanetti, 2012; Seymour, Burfoot, Smith, Cox, &Lockwood, 2002; Soria & Villamiel, 2010; Tiwari, Patras, Brunton,Cullen, & O’Donnell, 2010). In this context, this review focuses onapplication of ultrasound on fruit and vegetables.

2. History of ultrasound

Ultrasound has been used with different objectives, such ascommunication with animals, the location of flaws in concretebuildings, chemical synthesis and the diagnosis or treatment ofdiseases (Dolatowski, Stadnik, & Stasiak, 2007; Mason, 2003).

The discovery of ultrasound came with Pierre Curie in 1880 inhis studies of the piezoelectric effect (Shankar & Pagel, 2011). In1894, Thornycroft and Barnaby observed that vibrations weregenerated in the propulsion of missiles launched by a destroyer,which produced implosion bubbles and/or cavities in the water, aphenomenon known as cavitation (Martines, Davolos, & Júnior,2000).

Before World War II, applications of ultrasound were beingdeveloped for a range of technologies, including surface cleaningprocedures. In the 1960s, ultrasound technology was well estab-lished and used in cleaning and plastic welding (Mason, 2003).Despite the diverse applications and great development, ultra-sound science is still considered a recent technology. Sixty yearsago, low-intensity ultrasound methods were used to characterizefoods, but it is only recently that the potential of the method hasbeen evaluated (Dolatowski et al., 2007; Ulusoy, Colak, &Hampikyan, 2007).

3. Principles of ultrasound

Ultrasound is a form of energy generated by sound waves atfrequencies that are too high to be detected by the human ear.These waves participate in a region of the sound spectrum that isdivided into three main parts: infrasound (v < 16 Hz), band sound(16Hz < v < 16 kHz) and ultrasound (v > 16 kHz). The ultrasoundband is also divided into low frequency (16 kHz < v < 1 MHz) and

Fig. 1. Ultrasonic waves and the cavitation phenomenon.

J.F.B.de São José et al. / Food Control 45 (2014) 36e5038

high frequency (v > 1 MHz) bands. High-frequency ultrasoundbands are typically used for medical and industrial imaging pur-poses (Butz & Tauscher, 2002; Cárcel, García-Pérez, Benedito, &Mulet, 2012; Demirdöven & Baysal, 2009; Dolatowski et al., 2007;Kentish & Ashokkumar, 2011; Leadley &Williams, 2006; Sala, Raso,Pagán, & Condón, 1998).

Ultrasound can be classified by the energy amount used: Soundpower (W), sound intensity (W m�2) and sound energy density(Ws m�3) are the most significant measures used for categorizingultrasound applications (Knorr et al. 2004). Notably, the applica-tions of ultrasound are classified into low-energy (low power orlow intensity) and high-energy (high power or high intensity) ul-trasound (Kentish & Ashokkumar, 2011).

The low-energy group includes frequencies higher than 1 MHzand these ultrasonic waves cause no physical or chemical alter-ations in the properties of the material through which the wavepasses. Low-energy ultrasound produces non-destructive effectsand provides information about the physicochemical properties offoods, such as their composition, structure and physical state(Knorr et al. 2004; Leadley & Williams, 2006). High-power ultra-sound includes frequencies between 18 kHz and 100 kHz and canproduce physical, mechanical or chemical effects, such as thephysical disruption and acceleration of certain chemical reactions(Golmohamadi, Möller, Powers, & Nindo, 2013; Jayasooriya,Bhandari, Torley, & D’Arcy, 2004; Mason, 2003; São José &Vanetti, 2012).

High-intensity ultrasound has been used for many years toproduce emulsions, disrupt cells and disperse aggregatedmaterials.Diverse areas have been recognized for potential future develop-ment, for example, the adjustment and control of crystallizationprocesses; the measurement of texture, viscosity, and content ofsolids and fluids; the degassing of liquid foods; the inactivation ofenzymes; enhanced drying, filtration and induction of oxidationreactions and the inactivation of microorganisms (Knorr et al.2004; Suslick et al., 1999). The advantage using ultrasound is aconsequence of the various effects on themedium through which itis transmitted (Dolatowski et al., 2007).

Ultrasound is a technology used in the electronic industry todecontaminate surfaces and has been recommended for use in thefood industry (Cao et al., 2010; Chen & Zhu, 2011; Dolatowski et al.,2007; Kentish & Ashokkumar, 2011; Nascimento et al., 2008; Patist

& Bates, 2008). The physical effect can be the main action that isinvolved on microbial cell death. However, is known that the pro-duction of reactive compounds as peroxide hydrogen can be pro-moted the microbial disruption either (Gao, Lewis, Ashokkumar, &Hemar, 2014).

In food processing, high-intensity ultrasound at low frequencies,from 20 to 100 kHz, is useful in inactivating microorganisms(Piyasena, Mohareb, & McKellar, 2003). When propagated througha biological structure, ultrasound promotes the compression andexpansion of the medium particles, resulting in the production of ahigh amount of energy (Butz & Tauscher, 2002; Dolatowski et al.,2007; Kentish & Ashokkumar, 2011; Piyasena et al., 2003). Theinactivation of microorganisms is a consequence of cavitation.Cavitation (Fig. 1) is the formation, growth and collapse of bubblesthat generate a localized mechanical and chemical energy (Gogate& Kabadi, 2009; Rastogi, 2011).

When ultrasound waves pass through a liquid medium, me-chanical vibrations and acoustic streaming are generated withinthe liquid. Liquid media can contain dissolved gas, and they canexpand, promoting bubble formation and collapse through ultra-sound (Kentish & Ashokkumar, 2011). In addition, the violentcollapse events that occur during transient and repetitive transientcavitation can generate enormous localized temperatures (5500 K)and pressures (1000 MPa), or so-called hot spots, and release freeradicals as a result of the dissociation of vapour trapped in thebubbles. The occurrence of hot spots is limited in duration (Gabriel,2012; Knorr et al., 2004; Rastogi, 2011; Riener, Noci, Cronin,Morgan, & Lyng, 2009). It is important to discuss the hot spotsbecause if the treatment conditions are not well adjusted ratherthan to achieve a safe decontamination without damage to theplant, can be obtain rupture plant cell which culminates in loss ofquality original of the sanitized product (São José & Vanetti, 2012).

Increasing temperature and pressure changes can induce manychemical changes within both the vapour phase inside the cavita-tion bubble and the surrounding fluid (Kentish & Ashokkumar,2011; Piyasena et al., 2003). This phenomenon also generatesturbulence-located microcirculation. The implosions are asym-metric when produced near a solid surface, creating a microjet thathits the solid (Cárcel et al., 2012), and these changes contribute tothe mechanism used for cleaning surfaces (Bermúdez-Aguirre,Mobbs, & Barbosa-Cánovas, 2011; Gogate & Kabadi, 2009;

Fig. 2. Photomicrographs of Salmonella Typhimurium ATCC 14028 cells adhered to the surface of cherry tomatoes, imaged using scanning electron microscopy: non-sanitized (A),after sanitization with ultrasound for 10 min (B).

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 39

Piyasena et al. 2003; Rastogi, 2011). The amount of energy releasedby cavitation depends on the kinetics of the growth and collapse ofthe bubbles. Probably, these microjects contributed to remove theadhered bacteria cells on fruit and vegetable surfaces. This fact canoccur because the higher population of bacteria and the productionof exopolysaccharides became a barrier from sanitizers solutions(São José & Vanetti, 2012).

The ultrasound alone can provide powerful disinfection, but itsuse for large-scale microbiological decontamination should befurther evaluated, and in combination with other technologies, itcould even provide excellent results (Joyce, Phull, Lorimer, &Mason, 2003). The application of ultrasound individually or in

combination with peracetic acid was effective in removing Salmo-nella from the surface of cherry tomatoes (São José & Vanetti, 2012).The use of ultrasound has also been implemented in the disag-gregation of biofilms and the inactivation of microorganisms,which can help in the preservation of foods. Fig. 2 show that ul-trasound can remove adhered cells of Salmonella Typhimurium oncherry tomato surface.

Ultrasonic waves generate and distribute cavitation implosionsin liquid medium. The energy released during cavitation allowssurfaces that are generally difficult to access using other cleaningmethods to be reached (Gao et al., 2014). It is known that chemicalsanitizers are occasionally unsuccessful against microorganisms

J.F.B.de São José et al. / Food Control 45 (2014) 36e5040

that are present on biofilms or tightly adhered on surfaces. In thiscase, physical methods might be more helpful. Ultrasound is aconsistent and uniform method to remove contaminants. The useof ultrasound in the food industry is promising because a microbialbiofilm can occur on the surfaces of fruit and vegetables.

Ultrasound offers advantages in terms of cost, productivity andselectivity, with better processing time, improved quality, andreduced chemical damage and physical risks. Currently, the appli-cation of this technology has attracted attention for its role inenvironmental sustainability without causing damage, and it istherefore applicable to the concept of green technology (Chematet al., 2011).

3.1. Generation of power ultrasound

A power ultrasound system consists of three basic parts: anelectrical power generator, a transducer and a coupler/emitter(Mothibe et al., 2011).

The electrical generator is the source of energy for the ultra-sound system. Most generators allow the power to be set onlydirectly through voltage at current settings. These generators aretypically designed for industrial cleaning, therapeutic and dis-infecting applications (Leadley & Williams, 2006).

Transducers convert electrical energy through mechanical vi-brations at ultrasound frequencies. The main types of transducersinclude liquid-driven, magnetostrictive and piezoelectric transducers(Bérmudez-Aguirre et al., 2011). Liquid-driven transducers conductliquid across a thin metal blade, causing it to vibrate at ultrasonicfrequencies. With this transducer, rapidly alternating pressure andcavitation effects occur in the liquid, which generates a high degreeof mixing. This device is commonly used for the mixing and ho-mogenization process. Magnetostrictive transducers are electro-mechanical devices that use magnetostriction, an effect derivedfrom some ferromagnetic materials, which modifies dimension inresponse to the application of a magnetic field. The frequency rangeis typically restricted to below 100 kHz, and 60% of the electricalenergy was found to be re-allocated to acoustic energy because ofthe energy loss due to heat (Leadley &Williams, 2006). Piezoelectrictransducers are electrostrictive devices that use ceramic materials.Piezoceramic elements are the most common and efficient (80e95% transfer to acoustic energy) transducers (Leadley & Williams,2006). Piezoelectric transducers are not able to resist long expo-sures to high temperatures, for example, they cannot tolerate atemperature of 85 �C. These transducers are also used in diagnosisultrasound equipment (Rastogi, 2011).

The coupler or emitter, which is also called the reactor or ul-trasonic cell, is responsible for emitting the ultrasound waves fromthe transducer into the medium. The most important forms ofcouplers are bath couplers and horns/probes (Leadley & Williams,2006).

3.2. Available equipment

Many ultrasonic systems are available that primarily differ inthe power generator design, the transducer type used and thereactor to which it is coupled. The ultrasonic transducer (design,format and method) is important to define its effectiveness andefficiency, which is an important variable. Any differences be-tween laboratory and pilot plant designs and applications of ul-trasound can produce different results (Bérmudez-Aguirre et al.,2011).

Two different types of ultrasound equipment are typically usedin laboratories: ultrasonic cleaning baths and ultrasonic probes(Cárcel et al., 2012; Chemat et al., 2011; Mothibe et al., 2011).

Ultrasonic cleaning baths are commonly used for solid disper-sion, degassing solutions or cleaningmaterials (Fig. 3). They are lessused for chemical reactions, although they are inexpensive andeasy to use. Different capacities of this equipment are available.Typical tank sizes range from 10 to 2500 L (Awad, 2011). Ultrasonicbaths have transducers located on the walls and/or base of the tankand the ultrasonic energy is delivered directly to the liquid. Usually,this type of ultrasound operates at approximately 40 kHz andproduces high intensities at fixed levels. The depth of the liquid issignificant for maintaining these intensities and should not be lessthan half the wavelength of the ultrasound in the liquid. In theultrasonic bath, the frequencies are released through a mechanismthat produces a more uniform cavitation field and reduces sta-tionary wave zones (Cárcel et al., 2012; Chemat et al., 2011).

In the case of ultrasonic probes or horn systems, a rod-shapedmetal horn is used to amplify and conduct the high power acous-tic vibration in themedium. The horns or probes are frequently halfor multiple wavelengths in length. The gain in amplitude dependsupon the shape and variation in the diameter of the horn betweenthe driven face and the emitting face. This system is consideredmore powerful because the ultrasonic intensity is released from asmall surface at the extreme of the probe, and the probe can beimmersed into reaction flasks. However, this system can only beused on samples with small volumes, and careful attention must bepaid to the rapidly increasing temperature of the sample (Cárcelet al., 2012; Chemat et al., 2011).

However, laboratory studies can be adapted to allow large-scaleapplication using bath and flow ultrasound systems. Many ultra-sound systems have been designed for use in food processing. Forexample, an ultrasound bath can be used as a reactor for chickenshackles to avoid cross-contamination. Ultrasonic flow systems areused for liquid food, which is passed through a vibrating tube. Thesound energy generated for transducers bound to the outside of thetube is transferred directly into the flowing liquid (Mason, Riera,Vercet, & Lopez-Buesa, 2005).

Ultrasonic processing is becoming an important food-processing technology with a large commercial scale-up and suf-ficient returns on capital investments. Depending on the applica-tion, the energy required per litre of material treated (often definedas kWh/L) is similar to any other equipment in the industry, such asthat required for homogenization. Moreover, the equipment is easyto use because of the absence of moving parts (Patist & Bates, 2008).

Riera et al. (2004) discuss about use of airborne ultrasound andconclude that applications do exist provided that source must bevery powerful and efficient. This may be an option for fruits andvegetables that are highly perishable and should not be immersedin solutions.

Lin, Xu, and Hu (2011) proposed a new type of high powercomposite ultrasonic transducer that can be use in ultrasoniccleaning due the necessity of high power ultrasonic radiators withlarge radiating surfaces and powers. This transducer has a longi-tudinal sandwich transducer, two metal end masses, and a metalhollow cylinder that can radiate high power ultrasonic wave in thelongitudinal and the radial directions.

3.3. Factors affect ultrasound application in fresh fruit andvegetables

It is known that the extent of physical and chemical effects ofultrasound treatment are strongly associated with the amplitude ofultrasonic waves, exposure time, volume processed, food compo-sition and treatment temperature (Ananta, Voigt, Zenker, Heinz, &Knorr, 2005; Gómez-López, Orsolani, Martínez-Yépez, & Tapia,2010; Koda, Miyamoto, Toma, Matsuoka, & Maebayashi, 2009;

Fig. 3. Schematic illustration of ultrasound bath (1) and ultrasound probe (2).

Table 1Some causes and effects of ultrasound on microbial cell.

Causes Effect

Cavitation Cell wall structures are disruptedThinning of cellsCell wall is broken and releasing thecytoplasm contentPore formation, cell membrane disruption,and cell breakage

Free radicalproduction

DNA injures which produce breakages andfragmentation

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 41

Piyasena et al., 2003; Salleh-Mack & Roberts, 2007; Su, Zivanovic, &D’Souza, 2010; Tiwari et al., 2010).

Depending on the frequency used and sound wave amplitudeapplied, a number of physical, chemical and biochemical effects canbe observed with a variety of applications (Knorr et al., 2004). Thefrequency selected for the application affects the cavitation activity.The bubble size is inversely proportional to the frequency. Lowerfrequencies produce larger bubbles, and a higher energy is liber-ated. Ultrasonic waves with large amplitudes facilitate thedisplacement of molecules and collapse pressure (Povey & Mason,1998).

The effects produced by high power ultrasound when passedthrough a medium are diverse, and their relative importance de-pends on the characteristics of the food. The viscosity of the me-dium can affect cavitation. In highly viscous foods, ultrasounddiffusion is difficult, thus reducing the frequency at which cavita-tion occurs. Lower frequencies are more effective in this case, as theultrasound waves can pass through the viscous product(Bermúdez-Aguirre et al., 2011).

The pH of the medium or food is another condition that canaffect ultrasound efficiency. At a lower pH, inactivation rate ofmicroorganisms is increased. Salleh-Mack and Roberts (2007)studied the effect of pH on the inactivation of Escherichia coli andobserved a significant effect on the ultrasound inactivation (24 kHz/9 min), where a lower pH caused a major reduction in the count ofmicroorganisms. The same authors evaluated the presence of sol-uble solids at higher concentrations and observed that longer ul-trasound treatments were necessary to obtain the same reductionas observed in the treatment control. Then, the concentration ofsoluble solids in the medium had a protective effect.

Gera and Doores (2011) studied the kinetics and mechanism ofbacterial inactivation and the sonoprotective effect of milk com-ponents during the application of ultrasound (24 kHz at 30e35 �C)and observed that this food matrix exerts a protective effect onbacteria. Among the milk components tested, the presence oflactose showed higher D values, suggesting that lactose exerted aprotective effect on bacteria. These results suggest that when fresh-cut products are sanitized with ultrasound, some of the compoundsof these foods, such as exudates, can be released into the mediumand exert a protective effect on bacteria. Moreover, solid particlescan reduce the efficiency of cavitation.

The optimum temperature should be determined to enhancethe formation of cavitation. Salleh-Mack and Roberts (2007)observed that ultrasound (24 kHz/9 min) increased the sensitivity

of E. coli to thermal inactivation at increased temperatures. Thetemperature increase is not appropriate for minimally processedfruits and vegetables. Higher temperatures generated structuraland physiological alterations on vegetable tissue, whereas lowertemperatures reduced the respiration rate of fresh produce andminimised the loss of texture and other factors related to quality.

4. Microbial inactivation

The contamination of farm-raised vegetables and fruits mightoccur as a result of inadequate water irrigation, fertilizers, har-vesting, packaging, transport or handling at the point of sale. Sal-monella spp., Listeria monocytogenes, E. coli O157: H7, Aeromonasand the hepatitis A virus are some of the microorganisms associ-ated with contamination in foods, such as fruits and vegetables,which indicates the importance of controlling these pathogens as apublic health concern (Abadias, Usall, Anguera, Solsona, & Viñas,2008; Lapidot, Romling, & Yaron, 2006). The complete removaland/or inactivation of pathogens from the surfaces of fresh prod-ucts are a challenge for the food industry (São José & Vanetti, 2012).Thereby, new strategies to decontamination fruits and vegetablehave to be studied.

Several researches have been conducted to investigate themechanism of ultrasonic disruption in biological systems, andcavitation effects are considered to be a major factor. On Table 1 areexposed some causes and effects of ultrasound on microbial cell.

The mechanisms involved in cellular disruption are multifac-torial and might include shear forces generated during the move-ment of bubbles or sudden localized temperature and pressurechanges caused by bubble collapse (Salleh-Mack & Roberts, 2007;Ulusoy et al., 2007).

J.F.B.de São José et al. / Food Control 45 (2014) 36e5042

There are two types of cavitation, which have been observed tohave different effects. The first is stable cavitation, which occurs dueto oscillations of ultrasound waves, inducing the formation of tinybubbles in the liquid. The collapse of bubbles does not occur in thisprocess, but requires thousands of cycles of oscillating ultrasoundwaves to increase the bubble size (Cárcel et al., 2012). As the ul-trasonic wave passes through themedium, the bubbles vibrate, andcavitation sets up currents in the fluid adjacent to the vibratingbubbles; the currents in turn exert a twisting and rotational motionon near areas. Small bubbles travel through the sonic field andcreate microcurrents. This effect is called microstreaming. Nyborg(1982) describes microstreaming as a phenomenon that partici-pates in a class of acoustical occurrences, such as movements,forces, strains and stresses, in which the geometrical scale is small.This manifestation provides extensive forces, which rub against thesurface of cells and disrupt the cell membrane to induce thebreakdown of the cell wall. Nearby vibrating gas bubbles, rotationalforces and stresses affect intracellular organelles (Leadley &Williams, 2006). The second type is transient cavitation, wherebubbles increase in size within a few oscillatory cycles and thencollapse, causing cellular stress. Pressure can disrupt cell wallstructures, leading to cell leakage and disruption. Occasionalchanges in the pressure and temperature do not affect all cells, onlythose cells in the immediate proximity (Cárcel et al., 2012; Leadley& Williams, 2006).

Other proposed mechanisms of ultrasound on microbial inac-tivation occur by free radical formation. These compounds can helpfacilitate different applications of ultrasound. During bubblecollapse, energy is released, which can contribute to the sonolysisof water. In this reaction, OH�, Hþ and hydrogen peroxide aregenerated, which have important bactericidal effects. DNA is theprimary target of these free radicals in the bacterial cell, whichproduce breakages and fragmentation along the extension of theDNA (Bermúdez-Aguirre et al., 2011).

Stanley, Golden, Williams, and Weiss (2004) observed that anincreased hydrogen peroxide concentration induces a strongoxidation of lipid membranes, a disturbance in the enzymatic ac-tivity of protein complexes responsible for ATP production, and themaintenance of solute concentration in the cell interior, affectingthe genetic material. Disruption cell facilitates input of other sani-tizers as chlorine compounds that accelerates cell death.

The performance of ultrasound treatment is affected by theform, type or diameter of the microorganisms. It is important toknow what the target microorganism to choose the best treatmentconditions that will guarantee the method efficiency. Larger cellshave a larger surface area and are more sensitive than smaller ones(Ananta et al., 2005; Piyasena et al. 2003). Gram-positive bacteriaare recognised as more resistant than gram-negative bacteriabecause they have thicker cell walls that protect against the effectsof ultrasound. According to the literature, the differences in thesensitivity of the cells might also be due to a more tightly adherentlayer of peptidoglycan in gram-positive cells (Ananta et al., 2005;Piyasena et al. 2003; Ulusoy et al., 2007). Ultrasonic inactivationhas currently been associated with damage to the cell wall and cellwall structures, which is supported by the fact that some bacteriaare more resistant to cavitation than others under the same treat-ment conditions. The thinning of cell membranes together withheating and free radical production is essential for inactivation(Knorr et al., 2004; Ulusoy et al., 2007).

The outer membrane of gram-negative bacteria acts as a barrierand protects the cell. However, Ananta et al. (2005) observed thatultrasound (20 kHz/17�6 W) destabilizes the outer membrane andfacilitates the penetration of compounds. Moreover, ultrasound hasbeen associated with the enhanced inactivation of microorganismsin chemical solutions.

The effects of ultrasound on different bacteria remain ques-tionable. Scherba, Weigel, and O’Brien (1991) showed evidence ofno significant difference between the percentage of gram-positiveand gram-negative cells that are inactivated using ultrasound(26 kHz). Differences in the observed results mentioned could berelated to treatment conditions, such as the frequency or time ofapplication. The shape of cells can influence either the effectivenessof ultrasound. Alliger (1975) studied the effects of ultrasound oncells and found that spherical cells (cocci) are more resistant toultrasound than rod-shaped cells.

Pagán, Mañas, Álvarez, and Condón (1999) demonstrated thepotential of ultrasound (20 kHz) to inactivate pathogenic microor-ganisms, such as L. monocytogenes, which are found in outbreaks offood poisoning. However, Ulusoy et al. (2007) commented thatpathogens are resistant to different conditions of ultrasoundtreatment, particularly when used alone. Comparisons of differentresearch results are complicated, considering that conditions ofultrasound treatment can be different. Thus, it is important toobtain a careful and detailed evaluation of all treatment parametersbefore determining the effectiveness of a particular method onfruits and vegetables.

Although most studies are performed with ultrasound in liquidsystems (Guerrero, López-Malo, & Alzamora, 2001; Munkacsi &Elhami, 1976; San Martin, Harte, Lelieveld, Barbosa-Cánovas, &Swanson, 2001; Zenker, Heinz, & Knorr, 2003), it is known thatmicroorganism contaminants in solid foods can also be inactivatedusing this technology (Mason et al., 2005).

Limitations in reducing microorganisms from the surface offruits and vegetables might be associated with the occurrence ofthe multi-layered hydrophobic cuticle composed of cutin and waxmolecules that cover the epidermis, and this cuticle is highly re-pellent (Velázquez, Barbini, Escudero, & Estrada, 2009). Thus, ul-trasound has the potential to produce a deestabilization of bacteriabiofilms and can be used for the inactivation of bacteria (São José &Vanetti, 2012). However, Sengül, Erkaya, Baslar, and Ertugay (2011)proposed that this method was not effective in killing microor-ganisms in food at room or sublethal temperatures. Some re-searches show that the use of ultrasound alone can contribute todecontaminate. In fresh Tuber aestivum truffles, Rivera, Venturini,Oria, and Blanco (2011) observed that ultrasound (35 kHz/10 min)promotes the elimination of 1 log CFU g�1 of mesophilic microor-ganisms. Furthermore, others reports indicate that that ultrasoundis effective to inhibit the incidence of deterioration and preservesthe quality of post-harvest of fruits, as strawberries (Cao et al.,2010).

Ultrasound may be useful in the decontamination surface whenapplied in association with other method. Heat, high pressure, ul-traviolet radiation, pulsed electric field or chemical methods areoften used for cleaning and disinfection and can be applied incombination with ultrasound. In the case of fruits and vegetables,heat and pressure are not recommended for drastically altering thetissue structure of the plant. This review only discusses the com-bination of ultrasound with chemical compounds, such as com-mercial sanitizers, organic acids and others antimicrobials (Table 1).

Seymour et al. (2002) reported that the combination of ultra-sound (32e40 kHz/10 min) with sodium hypochlorite at 50 mg L�1

there was a further 1 log CFU g�1 reduction of S. Typhimurium inlettuce compared with ultrasound or chlorine solution alone. Kim,Feng, Kushad, and Fan (2006) studied the effects of ultrasound(40 kHz) on the germination of broccoli seeds and E. coli O157:H7and observed that none of the ultrasound treatments achievedmore than a 2 log cycle reduction in the E. coli population withoutlowering germination to below 85%.

Ferrante, Guerrero, and Alzamorat (2007) evaluated the addi-tional efficiency of the combination of vanillin, citral, and

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 43

ultrasound to inactivate L. monocytogenes in orange juice. Thecombination of high intensity ultrasound (20 kHz) with vanillin(500e1500 mg L�1) and citral (25e100 mg L�1) significantlyincreased L. monocytogenes inactivation.

Scouten and Beuchat (2002) found that the combination of ul-trasound (40 kHz) and Ca(OH)2 might be an alternative for thedecontamination of alfalfa sprouts inoculated with Salmonella andE. coli 0157: H7. Apples treated with ultrasound at a 170 kHz fre-quency combined with 20 mg L�1 chlorine dioxide showed a 4-logCFU g�1 reduction in the population of contaminating Salmonellaand E. coli O157: H7 (Huang et al., 2006). In addition, the populationof S. Typhimurium ATCC 14028 adhered to the surface of cherrytomatoes was reduced by approximately 4 log CFU g�1 in combi-nationwhen ultrasound (40 kHz) and peracetic acid were used (SãoJosé & Vanetti, 2012).

Zhou, Feng, and Luo (2009) observed that use of ultrasound(200W/L) contributed to a reduction of 0.7e1.1 log CFU g�1 of E. coliO157: H7 in spinach in all treatments compared with treatmentsusing only chemical sanitizers. Ayyildiz, Sanik, and Ileri (2011)observed that a sequential combination of ultrasound (20 kHz)and chlorinedioxideprovided a3.2e3.5 log reduction in thenumberof E. coli and total coliforms in rawwastewater, while the sum of thelog reductions using individual treatmentswere 1.4e1.9 log CFUmL.

Huang et al. (2006) investigated the decontamination efficacy ofthe combination of chlorine dioxide and ultrasound on apples andlettuce. Combining 10 min of ultrasound at 170 kHz and chlorinedioxide at 20 mg L�1 and 40 mg L�1 increased Salmonella reductionbymore than 2 log compared with the use of chlorine dioxide alonein apples. These results indicated that the association of ultrasoundwith other methods can result in a greater efficiency of sanitization.

Chen and Zhu (2011) demonstrated that the use of chlorine di-oxide in combination with ultrasound (40 kHz) allows the main-tenance of the post-harvest quality in the Japanese plum (Prunussalicina L.). Sagong et al. (2011) observed a synergistic effect in theuse of lactic acid (2%), citric acid (2%) and malic acid (2%) combinedwith ultrasound (40 kHz) for 5 min in the inactivation of E. coliO157: H7, S. Typhimurium and L. monocytogenes inoculated inorganic lettuces, without significantly affecting the colour andtexture.

These results indicate that ultrasound associated with othersanitizers is able to enhance the reduction of microbial flora indifferent products. However, the overall inactivation observedwhen ultrasound treatment is combined with antimicrobials de-pends on several factors, such as the type of antimicrobial agent,concentration and contact time. These details make it difficult toobtain general conclusions for other foods.

Other condition that ultrasound can be used for is to inactivationof endospores or spores. It is known that few species of bacteriahave the ability to produce highly these resistant structures. Thesestructures can resist to a range of hazardous conditions, such ashigh temperatures, osmotic pressures, extremes pH values, andmechanical shocks. Spores protect against heat, radiation anddehydration (Joyce et al., 2003). Some species, as Bacillus cereus iscommonly found on fruits and vegetables. B. cereus is a commonsoil inhabitant that can contaminate a variety of foods, such as rice,spices, milk and dairy products, vegetables, meat, cakes and otherdesserts. These bacteria produce several toxins and have beenisolated from sprouts and sprouting seeds (Kim et al., 2006) andfrom raw vegetables used to prepare minimally processed refrig-erated foods. The use of sanitizers to reduce spore bacteria levels infruits and vegetables has been proposed as a safety strategy. Bacillusand Clostridium spores are more resistant to sonication thanvegetative bacteria, and many of the heat-resistant bacteria aresimilarly resistant to ultrasound (Sanz, Palacios, Lopez, & Ordonez,1985). Sagong et al. (2013) observed that the most efficient

treatment for reducing B. cereus spores was the combination ofultrasound (40 kHz) and 0.1% Tween 20, yielding reductions of 2.49and 2.22 log CFU/g on lettuce and carrots, respectively, withoutcausing deterioration of quality.

Ultrasonic treatment, however, can induce changes in somecharacteristics of spores, such as swelling, surface erosion andgrowth stimulation (Burgos, Ordóñez, & Sala, 1972).

Studies have been conducted (Burgos et al., 1972) to evaluate theeffect of heat, pressure and ultrasonic waves on Bcillus subtilis.These studies were conducted in liquid medium and used othermethods of preservation that are not appropriate for fruits andvegetables. It is well understood that these methods can producediverse undesirable alterations in the natural characteristics offoods. Thus, more research is needed to evaluate the occurrence ofspores on fruits and vegetables and propose new technologies ofdecontamination.

Fruits and vegetables can also be contaminatedwithmoulds andyeasts. Fusarium, Alternaria and Phoma are toxigenic moulds thataffect plants, and these organisms can be transferred from diseasedplant parts to contaminate healthy plants. After harvesting, othermoulds could contaminate and spoil plant materials and producetoxic metabolites. Some of them could also produce mycotoxinswhile growing on these products, while others are pathogens thatpresent health hazards for the consumer (Tournas, 2005).

Synthetic chemical fungicides have been primarily used forreducing postharvest disease, mainly to control moulds on fruitsand vegetables. However, consumer concerns about pesticide res-idues on foods, along with pathogen resistance, have increased theneed to develop new methods to control postharvest diseases(Yang, Cao, Cai, & Zheng, 2011).

As Cao et al. (2010) showed, ultrasound (40 kHz) could beapplied to control decay and maintain the quality of fresh products.It is known that large postharvest losses occur as a consequence ofcontamination by moulds and yeast.

Yang et al. (2011) investigated the effect of ultrasound (40 kHz/10 min) and salicylic acid (0.05 mM) individually or in combinationon blue mould, which is caused by Penicillium expansum in peachfruit. The results showed that the combination of ultrasound withsalicylic acid was more effective than either individual treatment incontrolling postharvest blue mould in peach fruit.

Guerrero et al. (2001) conducted studies with ultrasound(20 kHz) for 20 min in Saccharomyces cerevisiae cells and observedthat the treatment punctured cells walls with a leakage of contentand damage at the inner cellular level. In this same study, the cellsappeared damaged in different forms, where some cells exhibited adisorganized inner structure or/rupture of the wall and plasmamembrane, while others cells did not. Cameron et al. (2008) eval-uated the effect of power ultrasound (20 kHz) on the survival ofthree microorganism types in UHT milk and observed damage tothe outer cell wall and inner cell membranes, and in the case ofyeast, internal damage to cell organelles was also observed.

Raw fruits and vegetables have frequently been involved in thefood-borne transmission of enteric viruses to humans. Amongthem, the Norovirus (NoV) and hepatitis A virus (HAV) arecurrently recognized as some of the most important human food-borne pathogens with regard to the number of outbreaks andpeople affected in the world (Fraisse et al., 2011). Although viralcontamination can occur during all steps of food processing, pri-mary production is a decisive stage at which prevention measuresmust be focused to minimize the risk of infection to consumers.Postharvest sanitation can be an important technological solutionfor decreasing the bacterial load on fresh raw material (Fraisseet al., 2011; Koopmans & Duizer, 2004). Thus, it is important toevaluate new methods, such as ultrasound, that can eliminateviruses.

J.F.B.de São José et al. / Food Control 45 (2014) 36e5044

Reports that evaluate the inactivation of viruses on fruits andvegetables using new technologies are scarce. Su et al. (2010)evaluated the effect of high intensity ultrasound on the infectivityof murine norovirus, feline calicivirus and MS2 bacteriophageinoculated in phosphate-buffered saline and orange juice. Theseauthors verified that the ultrasound effectiveness depended on thevirus type, the initial virus titre and the suspension solution. Theyalso concluded that ultrasound should be used in association withother methods to inactivate virus activity in food.

One justification for the difficult inactivation could be the smallcell size and genetic make-up (particularly single-stranded RNA) ofthe viruses studied; thus, the viruses were more resistant to thetechnologies applied.

In Table 2 are presented the results of several studies thatapplied ultrasound on fruits and vegetables to reduce microor-ganism count.

5. Effect of ultrasound on the properties of fruits andvegetables

Fruits and vegetables undergo a series of changes after harvestdue their environment, nutrient supply and injury during the

Table 2Ultrasound applications and microbial reductions in decontamination of some fruits and

Microorganism Conditions Food

Salmonella Typhimurium US þ 50 mg L�1 NaOCl LettuceE. coli 0157: H7Salmonella

US 40 kHz þ Ca(OH)2 1%treatment in bag

Alfalfa seeds

SalmonellaE. coli O157: H7

US 170 kHz þ 20 mg L�1 ClO2 Apples

Mesophilic aerobic US 20 kHzUS þ 100 mg L�1 Ca(ClO)2

Lettuce

E. coli O157:H7 US 40 kHz Broccoli seeds

E. coli O157: H7 US 200 W/L þ differentsanitizers

Spinach

Mesophilic aerobicMould and yeast

US 40 kHz Strawberry

E. coli O157: H7Salmonella TyphimuriumL. monocytogenes

US 40 kHz þ lactic acid (2%) Organic lettuces

Aerobic mesophilic bacteria US 40 kHz þ ClO2 Japanese plumMesophilic aerobic US 35 kHz Tuber aestivum trufflesPenicillium expansum US 40 kHz þ salicylic acid

(0.05 mM)Peach fruit

Salmonella TyphimuriumATCC 14028

US 40 kHz þ 40 mg L�1

peracetic acidCherry tomatoes

Bacillus cereus spores US 40 kHz þ 0.1% Tween 20 LettuceCarrots

E. coliS. aureusS. EnteritidisL. innocua

US 37 kHz Lettuce

E. coliS. aureusS. EnteritidisL. innocua

US 37 kHz Strawberry

E. coli O157:H7 US 40 kHz þ Electrolyzedwater þ immediatewater washing

Chinese CabbageLettuceSesame leafSpinach

L. monocytogenes US 40 kHz þ Electrolyzedwater þ immediatewater washing

Chinese CabbageLettuceSesame leafSpinach

US: ultrasound treatment.

harvesting process. Metabolism is modified but continues tofunction in live plant tissues. The intention of food preservationmethods is to extend the food’s shelf life through the inhibition ofdeleterious enzymatic reactions and microbial growth and thepreservation of nutritional and sensory aspects. Thus, it is impor-tant to evaluate the consequences of newmethods on the quality offruits and vegetables.

5.1. Inactivation of enzymes

The evaluation of enzymes and intermediate compounds of themain metabolic pathways or secondary routes can be excellentindicators of product quality, stress condition or physiological dis-order. The most important enzymes in fruits and vegetables areinvolved in taste and odour, such as lipoxygenase, lipases andproteases; texture is related to pectinases, b-glucosidases, cellu-lases, hemicellulases and peroxidase; colour is related to antho-cyanases, peroxidase, lipoxygenase, chlorophyillase andpolyphenoloxidase; and nutritional value is related to ascorbic acidoxidase, thiaminase and lipoxygenase (Lamikanra, 2002).

Studies evaluating the effects of ultrasound on the enzymespresent in fruits and vegetables are scarce. Most studies are

vegetables.

Time/�C Reduction References

10 min/not informed 1.2 log CFU g�1 Seymour et al. (2002)2 min/23 �C2 min/55 �C2 min/23 �C2 min/55 �C

1.021.612.283.27

Scouten and Beuchat (2002)

10 min/not informed 4 log CFU g�1

3.54 log CFU g�1Huang et al. (2006)

2 min/4 �C2 min/50 �C2 min/4 �C2 min/50 �C

0.90 log CFU g�1

0.98 log CFU g�1

1.02 log CFU g�1

1.35 log CFU g�1

Ajlouni et al. (2006)

30 min/23 �C5 min/55�C

1.04 log CFU g�1

1.44 log CFU g�1Kim et al. (2006)

2 min/not informed 0.7 to 1.1 log CFU g�1 Zhou et al. (2009)

10 min/20 �C 1.49 log CFU g�1

1.73 log CFU g�1Cao et al. (2010)

5 min/20 �C 2.75 log CFU g�1

2.71 log CFU g�1

2.50 log CFU g�1

Sagong et al. (2011)

10 min/20 �C 3.0 log CFU g�1 Chen and Zhu (2011)10 min/4 �C 1 log CFU g�1 Rivera et al. (2011)10 min/20 �C Reduce blue mould in

peach fruitYang et al. (2011)

10 min/24 �C 4 log CFU g�1 São José and Vanetti (2012)

5 min/20 �C 2.49 log CFU g�1

2.22 log CFU g�1Sagong et al. (2013)

30 min/not informed30 min/not informed30 min/not informed30 min/not informed

2.30 log CFU g�1

1.71 log CFU g�1

5.72 log CFU g�1

1.88 log CFU g�1

Birmpa et al. (2013)

30e45 min/not informed30e45 min/not informed30e45 min/not informed10 min/not informed

3.04 log CFU g�1

2.41 log CFU g�1

5.52 log CFU g�1

6.12 log CFU g�1

Birmpa et al. (2013)

3 min/23 � 2�C 2.60 log CFU g�1

2.50 log CFU g�1

2.33 log CFU g�1

2.41 log CFU g�1

Forghani and Oh (2013)

3 min/23 � 2�C 2.80 log CFU g�1

2.60 log CFU g�1

2.40 log CFU g�1

2.49 log CFU g�1

Forghani and Oh (2013)

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 45

conducted using liquid mediums or foods, such as fruit juices andmilk. Nevertheless, this article will discuss the effect of ultrasoundon important enzymes that are also present in fruits andvegetables.

The mechanism of enzyme inactivation by ultrasound is asso-ciated with cavitation through mechanical and chemical effects(Mañas, Muñoz, Sanz, & Condón, 2006; Raviyan, Zhang, & Feng,2005; Rawson, Tiwari, Patras, et al., 2011; Vercet, Burgos, Crelier,& Lopez-Buesa, 2001). When the bubbles collapse, high tempera-tures and shockwave pressures are generated. In addition to theseeffects, microstreaming is associated with high shear forces. Underthese intense conditions, ultrasound could induce the disruption ofhydrogen bonding and van der Waals interactions in polypeptidechains, leading to alterations of the secondary and tertiary struc-tures of the protein. The biological activities of enzymes are lost bythese modifications. The hot spots also lead to water moleculecleavage, generating high-energy intermediates, such as hydroxyland hydrogen-free radicals. The free radicals formed might reactwith some amino acid residues that participate in enzyme stability,substrate binding or catalytic function that consequently modifybiological activity (Mawson, Gamage, Terefe, & Knoerzer, 2011;Raviyan et al., 2005; Rawson, Tiwari, Patras, et al., 2011).

Some enzymes in food need to be inactivated to ensure themstabilization. The ultrasound inactivation of enzymes depends onproperties, such as frequency and power, and factors, such asenzyme type, concentration, medium pH, and temperature(Mawson et al., 2011; Raviyan et al., 2005; Tarun, Kurchenko, &Metelitza, 2006). Mawson et al. (2011) proposed that hydroxylradicals produced by cavitation events are less effective on en-zymes immobilized on the surfaces or within cells, such as those ofvegetable and fruit tissues. However, there is no evidence of thegenotoxic potential of ultrasound, as it is unclear whether extra-cellular or intracellular cavitation occurs.

Despite doubts about the effect of ultrasound in food enzymes,the possible effect of this method of food preservation in enzymaticactivity will be discussed. Lipoxygenase (LOX) is present in mostplant tissues, and in the presence of oxygen, it catalyses theoxidation of polyunsaturated fatty acids. Sterols and fatty acids areconstituents of cell membranes, and any change in the compositionof these compounds causes loss of fluidity. Lipid peroxidation caninduce the loss of membrane integrity. LOX causes undesirable ef-fects, such as the destruction of chlorophyll and carotenoids, thedevelopment of flavours and odours, and oxidative damage toproteins and vitamins (López et al., 1994). The undesirable odour invegetables is closely associated with the enzymatic peroxidation ofunsaturated fatty acids.

Lopez et al. (1994) evaluated the effect of ultrasound (20 kHz) onsoybean lipoxygenase buffer and observed a synergistic inactiva-tion effect between heat conditions and ultrasound. Minimallyprocessed fruits and vegetables are not subjected to heat treat-ment; therefore, it is useful to study the effect of ultrasound aloneor in combination with other non-thermal treatments on theinactivation of enzymes, such as lipoxygenase. It is important thatthe treatment does not cause changes in taste and odour in food.

López and Burgos (1995) reported a synergistic inactivation ef-fect that increased with amplitude with ultrasound treatment insoybean lipoxygenase buffer. These same authors showed thathydroxyl radicals have a short half-life and that their range of actionis short but can undergo radicaleradical combination reactions togenerate hydrogen peroxide. Hydrogen peroxide is an efficient LOX-inactivating factor, even at low concentrations and at roomtemperature.

Enzyme inactivation is a requisite for the stabilization of somefood materials (Vercert et al., 2001). Fruit enzymes can cause thedevelopment of brown colour and the loss of vitamin C, which

typically occurs in fruits that are served raw and are not subjectedto blanch treatment like vegetables.

Peroxidase (POD) is an enzyme commonly found in vegetables(Lamikanra, 2002). The presence of this enzyme is associated withoff flavours and off colours in raw and unblanched frozen vegeta-bles (González-Aguilar et al., 2005; Ruíz-Cruz, Islas-Osuna, Sotello-Mundo, Vázquez-Ortez, & González-Aguilar, 2007). POD inactiva-tion increases the shelf life of vegetables during frozen storage andcan be an index for blanching adequacy. Heat conditions can beused for enzyme inactivation, but these enzymes were heat resis-tant, and this treatment can modify several food properties, such asflavour, colour or nutritional value (Cruz, Vieira, & Silva, 2006;Lamikanra, 2002).

Ercan and Soysal (2011) used ultrasound to inactivate peroxi-dase in tomatoes. When ultrasound was applied for 150 s at 50%ultrasonic power, the inactivation of tomato POD was 100%. Poly-phenoloxidase (PPO) is an enzyme that participates in reactionsthat cause browning in fruits and vegetables (Ruíz-Cruz, Islas-Osuna, et al., 2007). Also known as catechol oxidase, diphenol ox-idase, o-diphenolase or phenolase tironase, PPO is found in mostfruits and vegetables, and the location of this enzyme in plant cellsdepends on the species, age and gradematurity. In green leaves, theenzyme is primarily found in chloroplasts (Lamikanra, 2002).

Softening is one of the most important changes usuallyobserved during fruit ripening (Ketsa & Daengkanit, 1999). The lossof firmness, however, is most often attributed to the enzymaticbreakdown of themiddle lamella and cell wall (Ketsa & Daengkanit,1999). A large number of enzymes participate in the degradation ofpectic substances, such as pectinmethylesterase, poly-galacturonase, b-galactosidase and cellulase.

Pectinmethylesterase (PME) is an endogenous pectic enzymethat has been identified primarily in the cell walls of vegetables cellthat de-esterifies the methyl group of pectin and converts it intolow methoxy pectin or pectic acids (Ketsa & Daengkanit, 1999;Lamikanra, 2002). The methoxy pectin or pectic acids can bedepolymerized and hydrolysed by PG, resulting in viscosity andtexture losses. To avoid quality losses, a partial or complete inac-tivation of PME together with the inactivation of PG is necessaryduring tomato processing (Raviyan et al., 2005). Pectin solubiliza-tion might contribute to loss from the cells walls, resulting insoftening during ripening. Raviyan et al. (2005) observed that ul-trasound (cavitationwasmensured by hydrogen peroxide yield rate0.004e0.020 mg L min�1) treatment effectively increased tomatoPME inactivation compared with a thermal treatment at the sametemperature. These authors related the increase of PME inactiva-tion with an increase in the cavitation intensity expressed by H2O2yield. This conclusion is consistent with Mawson et al. (2011), whoreported the importance of free radicals for enzyme inactivation.The development of polygalacturonase (PG) activity and softeningoccurred simultaneously in cherry, mango, papaya, pear and to-mato (Ketsa & Daengkanit, 1999; Lamikanra, 2002). PG hydrolysesglycosidic bonds between adjacent galacturonic acids, which arethe monomeric units of pectin (Vercet, Sánchez, Burgos, Montañés,& Buesa, 2002).

5.2. Effect on food components

There has been increasing consumer interest in functional foodwith basic nutrient functions and properties that can promotehealth and prevent diseases. Fruits and vegetables have theseproperties.

The content of these food compounds is strongly associatedwith their processing, manipulation and storage. Some studies haveshown that these operations have significant effects on the contentof bioactive compounds (Plaza et al., 2011; Rawson, Tiwari, Patras,

J.F.B.de São José et al. / Food Control 45 (2014) 36e5046

et al., 2011; Rawson, Tiwari, Tuohy, et al., 2011; Ruíz-Cruz, Islas-Osuna, et al., 2007; Soria & Villamiel, 2010; Vandekinderen et al.,2009). Fresh-cut produce deteriorates faster than intact produce,and this deterioration affects not only microbiological quality butalso nutritional and sensory quality. Therefore, we know thatbioactive compounds decrease as a consequence of deterioration.

It is known that to control microbial contamination in fruits andvegetables, it is necessary to use chemical or physical agents, suchas sanitizers. However, it is important that these processing stepsand postharvest treatments do not cause a significant reduction inthe produce’s nutrient content (Vandekinderen et al., 2008, 2009).These characteristics are relevant to a complete evaluation of theeffectiveness of the decontamination step.

The food industry is constantly searching for processing tech-nologies that allow the microbiological control of their productswithout changes in the nutritional and sensory characteristics offresh product. Studies assessing the effect on nutritional contentusing ultrasound are typically performed with fruit juices. How-ever, it is important to evaluate these parameters for productssubject to new processing technologies to allow a more accurateevaluation of the potential for application in food industry.

Some researchers have demonstrated the effect of commonsanitizers on the nutritional quality of fresh fruits and vegetables.Ruiz-Cruz et al. (2010) observed the reduction of vitamin C con-centration in fresh cut Jalapeno peppers after treatment withchlorinated solutions. Vandekideren et al. (2008) observed thatgaseous chlorine dioxide reduced both a and b-carotene in gratedcarrots. Pérez-Gregorio et al. (2011) studied sanitizing technologieson the loss of flavonoids and anthocyanins in onion slices andconcluded that onion flavonoids decreased using chemicallydisinfectant products and that ultrasound both maintained theinitial levels of flavonoids and subsequently increased them. Ruíz-Cruz, Islas-Osuna, et al., (2007) showed that different sanitizersdecrease carotene contents continuously during the storage ofcarrots. These results provided insight into the efficacy of physicalmethods, such as ultrasound, on these compounds.

During cavitation, hydroxyl radicals are produced, and thesecompounds can react with food compounds, but this interactioncan be beneficial or not, depending on the process and food matrix(Soria & Villamiel, 2010). It was reported that L-ascorbic acid wasdegraded by ultrasound treatment, possibly due to the generationof free radicals. However, during storage, ascorbic acid retention inultrasound-treated orange juicewas shown to be better than that ina thermally processed juice (Lee & Feng, 2011). Aadil, Zeng, Han,and Sun (2013) observed different results when evaluate effect ofsonication treatments on the contents of vitamin C of grapefruitjuice. In that research, was observed a significant increase invitamin C in all the sonicated juice samples (28 kHz, power set at70%) as compared to control. This increase in vitamin C can beattributed to the elimination of entrapped oxygen due to cavitation(Cheng, Soh, Liew, & Teh, 2007).

The degree of hydroxylation influences the activity of antioxi-dants in food and biological systems. Radical formation is consid-ered as a disadvantage for preserving the bioactivity of foodcomponents, such as phenolic compounds. Nevertheless, com-pounds such as flavonoids might enhance antioxidant activity byincreasing the extent of hydroxylation (Soria & Villamiel, 2010). It isan important to make the appropriate choice of ultrasound pa-rameters and conditions to treat fruit and vegetables withoutaffecting the nutrients.

Alexandre, Brandão, and Silva (2012) treated strawberries withnon-thermal technologies, such as ultrasound (35 kHz), andobserved higher anthocyanin contents than in samples washedwith chemical solutions when stored at room temperature for 6days. Tiwari, O’Donnell, Patras, Brunton, and Cullen (2009) studied

the stability of anthocyanins in sonicated (20 kHz) strawberry juiceduring storage and observed that this compound presented highlevels of retention. Tiwari et al. (2010) observed the significantretention of anthocyanins in grape juices after treatment with ul-trasound (at a constant frequency of 20 kHz and pulse durations of5 s on and 5 s off): 97.5% AC (cyanidin), 48.2%MA (malvanidina) and80.9% DA (delphinidin). Tiwari et al. (2009) commented that thedegradation of the anthocyanins might be related to oxidation re-actions promoted by the interaction of free radicals formed duringsonication.

Vitamin C is easily destroyed during the processing and storageof foods. The vitamin C content indicated a better quality of fruitand vegetables because it is a quality parameter and should bemaintained at an appropriate level (González-Aguillar et al., 2005).Ercan and Soysal (2011) observed that tomato juice treated withultrasound (23 kHz at 75% power for 90 s) and 12% of initial vitaminC is lost.

Tiwari et al. (2009) observed the retention of ascorbic acid instrawberry juice treated with ultrasound (20 kHz using a 1500 Wultrasonic processor). This result was attributed to the eliminationof dissolved oxygen during cavitations, which is essential forascorbic degradations.

Ascorbic acid retention reduced colour change during storage,which is appropriate because colour is associatedwith the selectionof fresh vegetables. The stability of vitamins is different from foodto food, even when they are subjected to similar processing andstorage.

Rawson, Tiwari, Patras, et al. (2011) studied the effect of ultra-sound (20 kHz) on vitamin C and carotenoids and concluded thatthis treatment was consistent with the retention of these com-pounds in carrots discs. Ashokkumar et al. (2008) suggested that thehydroxyl radicals generated during ultrasound treatment could beused to improve the degree of hydroxylation in food materials andhence increase the antioxidant activity of foods. However, it shouldbe noted that the generation of OH� radicalsmight affect the qualityof some foods by reducing the antioxidant capacity. Intense soni-cation is also known to generate off-flavours. Therefore, it isimportant to choose adequate conditions for applying ultrasoundtreatment tomaintainmicrobiological safetyandnutritional quality.

Bhat, Kamaruddin, Min-Tze, and Karim (2011) observed an in-crease in the total phenolic content in sonicated (25 kHz) kasturijuice samples compared with the control. Some studies, such asthat of Arzeni et al. (2012), evaluated the individual effect of ul-trasound on food components by applying high-intensive ultra-sound to food proteins. The results of that author indicated thatultrasound (20 kHz) induced modifications on functional proper-ties, such as viscosity and solubility, and those changes werebelieved to be associated with molecular modifications, such as ahydrophobicity increase and particle size variation. These changesdepend of the nature of protein and denaturation degree.

5.3. Sensory aspects

Some studies, such as the work of Vandekinderen et al. (2009),treated vegetables with chemical sanitizers and did not observe anychange in the sensory quality immediately after treatment. Ultra-sound has been studied as a method for the sanitization of fruitsand vegetables (Ajlouni, Sibrani, Premier, & Tomkins, 2006; Caoet al., 2010; Sagong et al., 2013; São José & Vanetti, 2012;Seymour et al., 2002; Zhuou et al., 2009). Data that can be foundin the literature explore the inactivation/removal of microorgan-isms and do not discuss their effects on the nutritional and sensorycharacteristics of fresh produce. Much of the data showed that ul-trasound and related effects on nutritional and sensory character-istics are the result of studies in liquid foods, such as juices and

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 47

milk. However, we discuss these results to understand the possiblechanges that could occur through the use of this method in fruitand vegetable sanitization.

The quality of fruits and vegetables is based on several proper-ties: texture, colour, flavour, and nutritional and functional char-acteristics. Biochemical transformations during the post-harvestdevelopment are primarily responsible for changes in the nutri-tional and sensory attributes of fruits and vegetables.

Fruit firmness is an important attribute that defines food quality.Texture is a physical characteristic that describes the responses tothe deformation of a liquid or solid food product. As a key foodquality attribute, texture is essentially determined by the micro-structure of the product. The texture of food treated by ultrasoundcan be determined by the structure or property changes of proteinsand enzymes during sonication.

In peppers, ultrasound (47 kHz) might injure the cell wallstructure and induce changes in the texture (Gabaldón-Leyva et al.,2007). However, Cao et al. (2010) observed that ultrasound treat-ment (40 kHz) inhibited the decrease of firmness in strawberries.Alexandre et al. (2012) treated strawberries with different sani-tizers and observed that samples treated with ultrasound (35 kHz)had 16% more firmness retention than the water-washed samples.These different observations should be due to different treatmentconditions as frequency, time, amplitude.

A restricted number of reports discuss the flavour changes infood treated with ultrasound. The free radicals produced by cavi-tation might catalyse the degradation of flavour compounds. Inother cases, such as wine, ultrasound can decrease the off-flavours(Lee & Feng, 2011).

The increase in volatile compounds is almost certainly due toreactions that take place during sonication treatment. It is uncer-tain that the nature of chemical reactions involved is specificallyassociated with only one or two of the components in a matrixchemically complex as milk (Riener et al., 2009).

Riener et al. (2009) observed that the long sonication (24 kHz) ofmilk produced volatile organic compounds that can be responsiblefor a “rubbery” aroma. This result shows that ultrasound-inducedreactions must be considered towards possibilities successfulintroduction of this technology in food industry. The composition offood and parameters of ultrasound influence the potential changesin the flavour of the final product.

The colour of a food product is an important freshness-relatedattribute for the consumer to use in evaluating the quality of theproduct. Disinfection agents possess strong oxidising propertiesassociated with deleterious effects on the colour of vegetables byinducing browning or bleaching of the vegetable tissue. Thermo-sonication (20 kHz) used in the blanching of watercress resulted indarker and less yellowish colours than in raw watercress (Cruz,Vieira, & Silva, 2006). Fava et al. (2011) treated grape berry fruitswith ultrasound (20 kHz) and observed that this treatment inducedsignificant differences in the colour parameters compared withuntreated fruit. Alexandre et al. (2012) treated strawberries withultrasound (35 kHz) for 2 min and observed better colour retentionthan in other treatments.

Aday, Temizkan, Büyükcan, and Caner (2013) verified that allultrasound treatments were effective to reduce mould growth and30 W and 60 W treatments maintained better textural propertiescompared with 90 W. As a result, it was concluded that powerlevels between 30 W and 60 W had improved quality and can beused to extend shelf life of strawberry.

6. Consumer acceptance

Consumers have been interested in products that havemicrobiological safety during production, a long shelf life, and

minimal changes in the nutritional and sensory quality of thefood (Rollin, Kennedy, & Wills, 2011). Such technologies, distinctof traditional processes, are aimed at reducing the loss of sensi-tive components, responsible for these sensory and nutritionalqualities.

Furthermore, new trends in technology should also seek toprotect the environment, showing concern for the balance betweenthe production and consumption of food. It is important thattechnologies do not impact the environment, such as in the form oftoxic by-products. These technologies are called “emerging tech-nologies” or “clean technologies”.

Sound waves are generally considered safe, non-toxic, andenvironmentally friendly, and this gives the use of ultrasound amajor advantage over other techniques. Studies confirming thepotential application in food industry show that these new tech-nologies and products should be evaluated and accepted for con-sumers. This evaluation will determine the commercial success orfailure of these products. Many factors can influence the con-sumer’s acceptance of food innovations. According to Rollin et al.(2011), the comprehension of risk-benefit perceptions of con-sumers, socio-demographic and economic factors, knowledge andinformation will be essential to the realization and success oftechnological advances.

7. Industrial uptake, status update and challenges faced bythe food industry

There is a great interest in ultrasound due to the fact that in-dustries can be provided with practical and consistent ultrasoundequipment. Currently, it is important to use a green novel tech-nology that has a role in the environment sustainability. Fruit andvegetables are washed typically with chlorine solutions. However,there is a tendency in eliminating chlorine based compounds fromthe decontamination process and applying novel and emergingtechnologies in the food industry. Researches indicated that ultra-sound can play an important role in fruit and vegetable decon-tamination. The adequate conditions, frequency, contact time andcombination of treatments for different decontamination technol-ogies are a challenge for the commercial application of ultrasound.More studies are required to use ultrasound technology fordecontamination purposes in food industry.

8. Conclusion

Ultrasound has potential applications for fresh fruits and vege-tables to control microbial contamination without changing theirquality aspects. Some studies have shown that ultrasound treat-ment could inactivate microorganisms and some enzymes. Theapplication of ultrasound can be effective when parameters (fre-quency, power, treatment time etc.) are adjusted to permit the ef-ficiency of sanitization without changing the nutritional andsensory quality of the food. The chemical and physical energygenerated by acoustic cavitation promotes severe damage to thecell wall, resulting in the inactivation of microorganisms. Thus,ultrasound can be a viable technique for quality assurance and foodsafety. Studies evaluating the use of ultrasound on fresh fruits andvegetables should be encouraged to provide a better understandingof the process and promote its application.

Acknowledgements

The authors thank CAPES for scholarship granted to firstauthor.

J.F.B.de São José et al. / Food Control 45 (2014) 36e5048

References

Aadil, R. M., Zeng, X., Han, Z., & Sun, D. (2013). Effects of ultrasound treatments onquality of grapefruit juice. Food Chemistry, 141(3), 3201e3206.

Abadias, M., Usall, J., Anguera, M., Solsona, C., & Viñas, I. (2008). Microbiologicalquality of fresh,minimally-processed fruit and vegetables and sprouts from retailestablishments. International Journal of Food Microbiology, 123(1e2), 121e129.

Aday, M. S., Temizkan, R., Büyükcan, M. B., & Caner, C. (2013). An innovative tech-nique for extending shelf life of strawberry: ultrasound. LWT e Food Science andTechnology, 52(2), 93e101.

Adekunte, A. O., Tiwari, B. K., Cullen, P. J., Scannell, A. G. M., & O’Donnell, C. P. (2010).Effect of sonication on colour, ascorbic acid and yeast inactivation in tomatojuice. Food Chemistry, 122(3), 500e507.

Adekunte, A., Tiwari, B. K., Scannell, A., Cullen, P. J., & O’Donnell, C. (2010). Modellingof yeast inactivation in sonicated tomato juice. International Journal of FoodMicrobiology, 137(1), 116e120.

Ajlouni, S., Sibrani, H., Premier, R., & Tomkins, B. (2006). Ultrasonication and freshproduce (Cos lettuce) preservation. Journal of Food Science, 71(2). M62e8.

Alexandre, E. M. C., Brandão, T. R. S., & Silva, C. L. M. (2012). Efficacy of non-thermaltechnologies and sanitizer solutions on microbial load reduction and qualityretention of strawberries. Journal of Food Engineering, 108(3), 417e426.

Allende, A., Selma, M. V., López-Gálvez, F., Villaescusa, R., & Gil, M. I. (2008). Impactof wash water quality on sensory and microbial quality, including Escherichiacoli cross-contamination, of fresh-cut escarole. Journal of Food Protection, 71(12),2514e2518.

Alliger, H. (1975). Ultrasonic disruption. American Laboratory, 10, 75e85.Alvaro, J. E., Moreno, S., Dianez, F., Santos, M., Carrasco, G., & Urrestarazu, M. (2009).

Effects of peracetic acid disinfectant on the postharvest of some fresh vegeta-bles. Journal of Food Engineering, 95(1), 11e15.

Ananta, E., Voigt, D., Zenker, M., Heinz, V., & Knorr, D. (2005). Cellular injuries uponexposure of Escherichia coli and Lactobacillus rhamnosus to high-intensity ul-trasound. Journal of Applied Microbiology, 99(3), 271e278.

Artés, F., & Allende, A. (2005). Minimal fresh processing of vegetables, fruits andjuices. In D. W. Sun (Ed.), Emerging technologies for food processing (pp. 677e716). California: Elsevier Academic Press.

Arzeni, C., Martínez, K., Zema, P., Arias, A., Pérez, O. E., & Pilosof, A. M. R. (2012).Comparative study of high intensity ultrasound effects on food proteins func-tionality. Journal of Food Engineering, 108(3), 463e472.

Ashokkumar, M., Sunartio, D., Kentish, S., Mawson, R., Simons, L., Vilkhu, K., et al.(2008). Modification of food ingredients by ultrasound to improve function-ality: a preliminary study on a model system. Innovative Food Science andEmerging Technologies, 9(2), 155e160.

Awad, S. B. (2011). Higher-power ultrasound in surface cleaning and decontami-nation. In H. Feng, G. V. Barbosa-Cánovas, & J. Weiss (Eds.), Ultrasound tech-nologies for food and bioprocessing (pp. 545e558). New York: Springer.

Ayyildiz, O., Sanik, S., & Ileri, B. (2011). Effect of ultrasonic pretreatment on chlorinedioxide disinfection efficiency. Ultrasonics Sonochemistry, 18(2), 683e688.

Bermúdez-Aguirre, D., Mobbs, T., & Barbosa-Cánovas, G. V. (2011). Ultrasound ap-plications in food processing. In H. Feng, G. V. Barbosa-Cánovas, & J. Weiss(Eds.), Ultrasound technologies for food and bioprocessing (pp. 64e105). NewYork: Springer.

Bhat, R., Kamaruddin, N. S. B. C., Min-Tze, L., & Karim, A. A. (2011). Sonication im-proves kasturi lime (Citrus microcarpa) juice quality. Ultrasonics Sonochemistry,18, 1295e1300.

Birmpa, A., Sfika, V., & Vantakaris, A. (2013). Ultraviolet light and ultrasound as nonthermal treatments for inactivation of micro-organisms in fresh read-to-eatfoods. International Journal of Food Microbiology, 167(1), 96e102.

Burgos, J., Ordóñez, J. A., & Sala, F. (1972). Effect of ultrasonic waves on the heatresistance of Bacillus cereus and Bacillus licheniformis spores. Applied Microbi-ology, 24(3), 497e498.

Butz, P., & Tauscher, B. (2002). Emerging technologies: chemical aspects. FoodResearch International, 35(2e3), 279e284.

Cameron, M., McMaster, L. D., & Britz, T. J. (2008). Electron microscopic analysis ofdairymicrobes inactivatedbyultrasound.Ultrasonics Sonochemistry,15, 960e964.

Cao, S., Hu, Z., Pang, B., Wang, H., Xie, H., & Wu, F. (2010). Effect of ultrasoundtreatment on fruit decay and quality maintenance in strawberry after harvest.Food Control, 21(4), 529e532.

Cárcel, J. A., García-Pérez, J. V., Benedito, J., & Mulet, A. (2012). Food process inno-vation through new technologies: use of ultrasound. Journal of Food Engineering,110(2), 200e207.

Chemat, F., & Hoarau, N. (2004). Hazard analysis and critical control point (HACCP)for an ultrasound food processing operation. Ultrasonics Sonochemistry, 11(3e4),257e260.

Chemat, F., Zill-e-huma, & Khan, M. K. (2011). Applications of ultrasound in foodtechnology: processing, preservation and extraction. Ultrasonic Sonochemistry,18(4), 813e835.

Chen, Z., & Zhu, C. (2011). Combined effects of aqueous chlorine dioxide and ul-trasonic treatments on postharvest storage quality of plum fruit (Prunus salicinaL.). Postharvest Biology and Technology, 61(2e3), 117e123.

Cheng, L. H., Soh, C. Y., Liew, S. C., & Teh, F. F. (2007). Effects of sonication andcarbonation on guava juice quality. Food Chemistry, 104, 1396e1401.

Cruz, R. M. S., Vieira, M. C., & Silva, C. L. M. (2006). Effect of heat and thermoso-nication treatments on peroxidase inactivation kinetics in watercress (Nastur-tium officinale). Journal of Food Engineering, 72(1), 8e15.

Demirdöven, A., & Baysal, T. (2009). The use of ultrasound and combined tech-nologies in food preservation. Food Reviews International, 25(1), 1e11.

Dolatowski, Z. J., Stadnik, J., & Stasiak, D. (2007). Applications of ultrasound in foodtechnology. Acta Scientarium Polonorum Technology Alimentaria, 6(3), 89e99.

Ercan, S. S., & Soysal, C. (2011). Effect of ultrasound and temperature on tomatoperoxidase. Ultrasonics Sonochemistry, 18(2), 686e695.

Fava, J., Hodara, K., Nieto, A., Guerrero, S., Alzamora, S. M., & Castro, M. A. (2011).Structure (micro, ultra, nano), color and mechanical properties of Vitis labruscaL. (grape Berry) fruits treated by hydrogen peroxide, UV-C irradiation and ul-trasound. Food Reasearch International, 44(9), 594e595.

Ferrante, S., Guerrero, S., & Alzamorat, S. M. (2007). Combined use of ultrasoundand natural antimicrobials to inactivate Listeria monocytogenes in orange juice.Journal of Food Protection, 70, 1850e1857.

Forghani, F., & Oh, D.-H. (2013). Hurdle enhancement of slightly acidic electro-lyzed water antimicrobial efficacy on Chinese cabbage, lettuce, sesame leafand spinach using ultrasonication and water wash. Food Microbiology, 36(1),40e49.

Fraisse, A., Temmam, S., Deboosere, N., Guillier, L., Delobel, A., Maris, P., et al. (2011).Comparison of chlorine and peroxyacetic-based disinfectant to inactivate Felinecalicivirus, Murine norovirus and Hepatitis A virus on lettuce. InternationalJournal of Food Microbiology, 151(1), 98e104.

Gabaldón-Leyva, C. A., Quintero-Ramos, A., Barnard, J., Balandrán-Quintana, R. R.,Talamás-Abbud, R. T., & Jiménez-Castro, J. (2007). Effect of ultrasound on themass transfer and physical changes in brine bell pepper at different tempera-ture. Journal of Food Engineering, 81, 374e379.

Gabriel, A. A. (2012). Microbial inactivation in cloudy apple juice by multi-frequencyDynashock power ultrasound. Ultrasonics Sonochemistry, 19(2), 346e351.

Gao, S., Lewis, G. D., Ashokkumar, M., & Hemar, Y. (2014). Inactivation of microor-ganisms by low-frequency high-power ultrasound: 1. Effect of growth phaseand capsule properties of the bacteria. Ultrasonics Sonochemistry, 21, 446e453.

Gera, N., & Doores, S. (2011). Kinetics and Mechanism of bacterial inactivation byultrasound waves and sonoprotective effect of milk components. Journal of FoodScience, 76(2), m111em119.

Gogate, P. R., & Kabadi, A. M. (2009). A review of applications of cavitation inbiochemical engineering/biotechnology. Biochemical Engineering Journal, 44(1),60e72.

Golmohamadi, A., Möller, G., Powers, J., & Nindo, C. (2013). Effect of ultrasoundfrequency on antioxidant activity, total phenolic and anthocyanin content of redraspberry puree. Ultrasonics Sonochemistry, 20(5), 1316e1323.

Gómez-López, V. M., Orsolani, L., Martínez-Yépez, A., & Tapia, M. S. (2010). Micro-biological and sensory quality of sonicated calcium-added orange juice. LWT-Food Science and Technology, 43(5), 808e813.

González-Aguillar, G. A., Ruíz-Cruz, S., Soto-Valdez, H., Vásquez-Ortiz, F., Pacheco-Aguilar, R., & Wang, C. Y. (2005). Biochemical changes of fresh-cut pineappleslices treated with antibrowning agents. International Journal of Food Scienceand Technology, 40(4), 377e383.

Guerrero, S., López-Malo, A., & Alzamora, S. M. (2001). Effect of ultrasound on thesurvival of Saccharomyces cerevisiae: influence of temperature, pH and ampli-tude. Innovative Food Science an Emmerging Technologies, 2(1), 31e39.

Huang, T. S., Xu, C., Walker, K., West, P., Zhang, S., & Weese, J. (2006). Decontami-nation efficacy of combined chlorine dioxide with ultrasonication on apples andlettuce. Journal of Food Science, 71(4), m134em139.

Jayasooriya, S. D., Bhandari, B. R., Torley, P., & D’Arcy, B. R. (2004). Effect of highpower ultrasound waves on properties of meat: a review. International Journalof Food Properties, 7(2), 301e319.

Joyce, E., Phull, S. S., Lorimer, J. P., & Mason, T. J. (2003). The development andevaluation of ultrasound for the treatment of bacterial suspensions. A study offrequency, power and sonication time on cultured Bacillus species. UltrasonicsSonochemistry, 10(6), 315e318.

Kentish, S., & Ashokkumar, M. (2011). The physical and chemical effects of ultra-sound. In H. Feng, G. V. Barbosa-Cánovas, & J. Weiss (Eds.), Ultrasound tech-nologies for food and bioprocessing (pp. 1e12). New York: Springer.

Ketsa, S., & Daengkanit, T. (1999). Firmness and activities of polygalacturonase,pectinesterase, b-galactosidase and cellulose in ripening durian harvest atdifferent stages of maturity. Scientia Horticulturae, 80(1), 181e188.

Kim, H. J., Feng, H., Kushad, M. M., & Fan, X. (2006). Effects of ultrasound, irradiationand acidic electrolyzed water on germination of alfalfa and broccoli seeds andEscherichia coli O157:H7. Journal of Food Science, 71(6), m168em173.

Knorr, D., Zenker, M., Heinz, V., & Lee, D. U. (2004). Applications and potential of ul-trasonics in food processing. Trends in Food Science and Technology,15(5), 261e266.

Koda, S., Miyamoto, M., Toma, M., Matsuoka, T., & Maebayashi, M. (2009). Inacti-vation of Escherichia coli and Streptococcus mutans by ultrasound at 500 kHz.Ultrasonics Sonochemistry, 16, 655e659.

Koopmans, M., & Duizer, E. (2004). Foodborne viruses: an emerging problem. In-ternational Journal of Food Microbiology, 90(1), 23e41.

Lamikanra, O. (2002). Enzymatic effects on flavor and texture of fresh-cut fruits andvegetables. In O. Lamikanra (Ed.), Fresh cut fruits and vegetables: Science, tech-nology and market. Washington DC: Ed. CRC Press.

Lapidot, A., Romling, U., & Yaron. (2006). S. Biofilm formation and the survival ofSalmonella Typhimurium on parsley. International Journal of Food Microbiology,109(3), 229e233.

Leadley, C. E., & Williams, A. (2006). Pulsed electric field processing, power ultra-sound and other emerging technologies. In James G. Brennan (Ed.), Food pro-cessing handbook. Weinheim: Wiley-Vch Verlag GmbH & Co. KGaA.

J.F.B.de São José et al. / Food Control 45 (2014) 36e50 49

Lee, H., & Feng, H. (2011). Effect of power ultrasound on food quality. In H. Feng,G. V. Barbosa-Cánovas, & J. Weiss (Eds.), Ultrasound technologies for food andbioprocessing (pp. 559e582). New York: Springer.

Lin, S., Xu, L., & Hu, W. (2011). A new type of high power composite ultrasonictransducer. Journal of Sound and Vibration, 330(7), 1419e1431.

Lopez, P., & Burgos, J. (1995). Peroxidase stability and reactivation after heattreatment and monothermosonication. Journal of Food Science, 60(3), 451e455.

Lopez, P., Sala, F. J., De La Fuente, J. L., Condon, S., Raso, J., & Burgos, J. (1994).Inactivation of peroxidase, lipoxygenase, and polyphenol oxidase by man-othermosonication. Journal of Agricultural and Food Chemistry, 42, 252e256.

Mañas, P., Muñoz, B., Sanz, D., & Condón, S. (2006). Inactivation of lysozyme byultrasonic waves under pressure at different temperatures. Enzyme and Mi-crobial Technology, 39(6), 1177e1182.

Martines, M. A. U., Davolos, M. R., & Júnior, M. J. (2000). O efeito do ultra-som emreações químicas. Química Nova, 23(2), 251e256.

Martinéz-Sánchez, A., Allende, A., Bennett, R. N., Ferreres, F., & Gil, M. I. (2006).Microbial, nutritional and sensory quality of rocket leaves as affected bydifferent sanitizers. Postharvest Biology and Technology, 42(1), 86e89.

Mason, T. J. (2003). Sonochemistry and sonoprocessing: the link, the trends and(probably) the future. Ultrasonics Sonochemistry, 10(4e5), 175e179.

Mason, T., Riera, E., Vercet, A., & Lopez-Buesa, P. (2005). Application of ultrasound.In D. W. Sun (Ed.), Emerging technologies for food processing (pp. 323e350).California: Elsevier Academic Press.

Mawson, R., Gamage, M., Terefe, N. S., & Knoerzer, K. (2011). Ultrasound in enzymeactivation and inactivation. In H. Feng, G. V. Barbosa-Cánovas, & J. Weiss (Eds.),Ultrasound technologies for food and bioprocessing (pp. 369e404). New York:Springer.

Mothibe, K. J., Zhang, M., Nsor-Atindana, J., & Wang, Y. (2011). Use of ultrasoundpretreatment in drying of fruits: drying rates, quality attributes, and shelf lifeextension. Drying Technology, 29(14), 1611e1621.

Munkacsi, F., & Elhami, M. (1976). Effect of ultrasonic and ultraviolet irradiation onchemical and bacteriological quality of milk. Egyptian Journal of Dairy Science,4(1), 1e6.

Nascimento, L. C., Lima, L. C. O., Picolli, R. H., Fiorini, J. E., Duarte, S. M. S., et al.(2008). Ozônio e ultrassom: processos alternativos para o tratamento do cafédespolpado. Revista Ciência e Tecnologia de Alimentos, 28(2), 282e294.

Nyborg, W. L. (1982). Ultrasonic microstreaming and related phenomena. The BritishJournal of Cancer Supplement, 5(1), 156e160.

Pagán, R., Mañas, P., Álvarez, I., & Condón, S. (1999). Resistance of Listeria mono-cytogenes to ultrasonic waves under pressure at sublethal (manosonication) andlethal (manothermosonication) temperatures. Food Microbiology, 16(2), 139e148.

Patil, S., Bourke, P., Kelly, B., Frías, J. M., & Cullen, P. J. (2009). The effects of acidadaptation on Escherichia coli inactivation using power ultrasound. InnovativeFood Science & Emerging Technologies, 10(4), 486e490.

Patist, A., & Bates, D. (2008). Ultrasonic innovations in the food industry: from thelaboratory to commercial production. Innovative Food Science and EmergingTechnology, 9(2), 147e154.

Pérez-Gregorio, M. R., González-Barreiro, C., Rial-Otero, R., & Simal-Gándara, J.(2011). Comparison of sanitizing technologies on the quality appearance andantioxidant levels in onion slices. Food Control, 22(12), 2052e2058.

Piyasena, P., Mohareb, E., & McKellar, R. C. (2003). Inactivation of microbes usingultrasound: a review. International Journal of Food Microbiology, 87(3), 207e216.

Plaza, L., Crespo, I., Pascual-Teresa, S., De Ancos, B., Sánchez-Moreno, C., Muñoz, M.,et al. (2011). Impact of minimal processing on orange bioactive compoundsduring refrigerated. Food Chemistry, 124(2), 646e651.

Povey, M., & Mason, T. (1998). Ultrasound in food processing. London: Blackie Aca-demic and Professional.

Rastogi, N. (2011). Opportunities and challenges in application of ultrasound in foodprocessing. Critical Reviews in Food Science and Nutrition, 51(8), 705e722.

Raviyan, P., Zhang, Z., & Feng, H. (2005). Ultrasonication for tomato pectinmethy-lesterase inactivation: effect of cavitation intensity and temperature on inac-tivation. Journal of Food Engineering, 70(2), 189e196.

Rawson, A., Tiwari, B. K., Patras, A., Brunton, N., Brennan, C., Cullen, P. J., et al. (2011).Effect of thermosonication on bioactive compounds in watermelon juice. FoodResearch International, 44(5), 1168e1173.

Rawson, A., Tiwari, B. K., Tuohy, M. G., O’Donnel, C. P., & Brunton, N. (2011). Effect ofultrasound and blanching pretreatments on polyacetylene and carotenoidcontent of hot air and freeze dried carrots discs. Ultrasonics Sonochemistry, 18(5),1172e1179.

Rico, D., Martín-Diana, A. B., Barat, J. M., & Barry-Ryan, C. (2007). Extending andmeasuring the quality of fresh-cut fruit and vegetables: a review. Trends in FoodScience and Technology, 18(7), 373e386.

Riener, J., Noci, F., Cronin, D. A., Morgan, D. J., & Lyng, J. G. (2009). Characterisation ofvolatile compounds generated in milk by high intensity ultrasound. Interna-tional Dairy Journal, 19(4), 269e272.

Riera, E., Golás, Y., Blanco, A., Gallego, J. A., Blasco, M., & Mulet, A. (2004). Masstransfer enhancement in supercritical fluids extraction by means of power ul-trasound. Ultrasonics Sonochemistry, 11(3(4)), 241e244.

Rivera, C. S., Venturini, M. E., Oria, R., & Blanco, D. (2011). Selection of a decon-tamination treatment for fresh Tuber aestivum and Tuber melanosporum trufflespackaged in modified atmospheres. Food Control, 22(3e4), 626e632.

Rollin, F., Kennedy, J., & Wills, J. (2011). Consumers and new technologies. Trends inFood Science & Technology, 22(2e3), 99e111.

Ruiz-Cruz, S., Alvarez-Parrilla, E., de la Rosa, L. A., Martinez-Gonzalez, A. I., Ornelas-Paz, J., Mendoza-Wilson, A. M., et al. (2010). A. Effect of different sanitizers on

microbial, sensory and nutritional quality of fresh-cut jalapeno peppers. Journalof Agriculture and Biological Science American, 5, 331e341.

Ruíz-Cruz, S., Félix, E. A., Diáz-Cinco, M., Islas-Osuna, M. A., & González-Aguilar, G. A.(2007). Efficacy of sanitizers in reducing Escherichia coli O157:H7, Salmonellaspp. and Listeria monocytogenes populations on fresh-cut carrots. Food Control,18(11), 1383e1390.

Ruíz-Cruz, S., Islas-Osuna, M. A., Sotello-Mundo, R., Vázquez-Ortez, F., & González-Aguilar, G. A. (2007). Sanitation procedure affects biochemical and nutritionalchanges of shredded carrots. Journal of Food Science, 72(2), s146es152.

Sagong, H. G., Cheon, H.-L., Lee, S. Y., Park, K. H., Chung, M. S., Ryu, S., et al. (2013).Combined effects of ultrasound and surfactants to reduce Bacillus cereus sporeson lettuce and carrots. International Journal of Food Microbiology, 160(3), 367e372.

Sagong, H. G., Lee, S.-Y., Chang, P. S., Heu, S., Ryu, S., Choi, Y. J., et al. (2011). Com-bined effect of ultrasound and organic acids to reduce Escherichia coli O157:H7,Salmonella Typhimurium, and Listeria monocytogenes on organic fresh lettuce.International Journal of Food Microbiology, 145(1), 287e292.

Sala, F. J., Raso, J., Pagán, R., & Condón, S. (1998). Influence of temperature andpressure on the lethality of ultrasound. Applied and Environmental Microbiology,465e471.

Salleh-Mack, S. Z., & Roberts, J. S. (2007). The effects of temperature, soluble solids,organic acids and pH on the inactivation of Escherichia coli ATCC 25922. Ul-trasonics Sonochemistry, 14(3), 323e329.

San Martín, M. F., Harte, F. M., Lelieveld, H., Barbosa-Cánovas, G., & Swanson, B. G.(2001). Inactivation effect of 18 pulsed magnetic field combined with anothertechnologies on Escherichia coli. Innovative Food Science and Emerging Technol-ogies, 2(1), 273e277.

Sanz, P., Palacios, P., Lopez, P., & Ordonez, J. A. (1985). Effect of ultrasonic waves onthe heat resistance of Bacillus stearothermophilus spores. In D. J. E. Dring, &G. W. Gould (Eds.), Fundamental and applied aspects of bacterial spores (pp. 251e259). New York: Academic Press.

São José, J. F. B., & Vanetti, M. C. D. (2012). Effect of ultrasound and commercialsanitizers on natural microbiota and Salmonella enterica Typhimurium oncherry tomatoes. Food Control, 24(1e2), 95e99.

Scherba, G., Weigel, R. M., & O’Brien, J. R. (1991). Quantitative assessment of thegermicidal efficiency of ultrasonic energy. Applied Environmental Microbiology.,57(1), 2079e2084.

Scouten, A. J., & Beuchat, L. R. (2002). Combined effects of chemical and ultrasoundtreatments to kill Salmonella and Escherichia coli O157:H7 on alfalfa seeds.Journal of Applied Microbiology, 92(4), 668e674.

Selma, M. V., Ibáñez, A. M., Allende, A., Cantwell, M., & Suslow, T. (2008). Effect ofgaseous ozone and hot water on microbial and sensory quality of cantaloupeand potential transference of Escherichia coli O157:H7 during cutting. FoodMicrobiology, 25(1), 162e168.

Sengül, M., Erkaya, T., Baslar, M., & Ertugay, M. F. (2011). Effect of photosonicationtreatment on inactivation of total and coliform bacteria in milk. Food Control,22(11), 1803e1806.

Seymour, I. J., Burfoot, D., Smith, R. L., Cox, L. A., & Lockwood, A. (2002). Ultrasounddecontamination of minimally processed fruits and vegetables. InternationalJournal of Food Science and Technology, 37(1), 547e557.

Shankar, H., & Pagel, P. S. (2011). Potential adverse ultrasound-related biologicaleffects: a critical review. Anesthesiology, 115(5), 1109e1124.

Soria, A. C., & Villamiel, M. (2010). Effect of ultrasound on the technological prop-erties and bioactivity of food: a review. Trends in Food Science & Technology,21(7), 323e331.

Stanley, K. D., Golden, D. A., Williams, R. C., & Weiss, J. (2004). Inactivation ofEscherichia coli O157:H7 by high-intensity ultrasonication in the presence ofsalts. Foodborne Pathogens and Disease, 1(1), 267e273.

Suslick, K. S., Didenko, Y., Fang, M. M., Hyeon, T., Kolbeck, K. J., McNamara, W. B., III,et al. (1999). Acoustic cavitation and its chemical consequences. PhilosophicalTransactions of the Royal Society A, 357(1751), 335e353.

Su, X., Zivanovic, S., & D�Souza, D. H. (2010). Inactivation of human enteric virussurrogates by high-intensity ultrasound. Foodborne Pathogens and Disease, 7(9),1e7.

Tarun, E. I., Kurchenko, V. P., & Metelitza, D. I. (2006). Flavonoids as effective pro-tectors of urease from ultrasonic inactivation in solutions. Russian Journal ofBioorganic Chemistry, 32(4), 352e359.

Tiwari, B. K., O’Donnell, C. P. O., Patras, A., Brunton, N., & Cullen, P. J. (2009). Stabilityof anthocyanins and ascorbic acid in sonicated strawberry juice during storage.European Food Research Technology, 228(5), 717e724.

Tiwari, B. K., Patras, A., Brunton, N., Cullen, P. J., & O’Donnell, C. P. (2010). Effect ofultrasound processing on anthocyanins and color of red grape juice. UltrasonicsSonochemistry, 17(3), 598e604.

Tournas, V. H. (2005). Molds and yeasts in fresh and minimally processed vegeta-bles, and sprouts. International Journal of Food Microbiology, 99(1), 71e77.

Ulusoy, B. H., Colak, H., & Hampikyan, H. (2007). The use of ultrasonic waves in FoodTechnology. Research Journal of Biological Sciences, 2(4), 491e497.

Vandekinderen, I., Camp, J. V., De Meulenar, B., Veramme, K., Bernaert, N., Denon, Q.,et al. (2009). Moderate and high doses of sodium hypochlorite, neutral elec-trolyzed oxidizing water, peroxyacetic acid, and gaseous chlorine dioxide didnot affect the nutritional and sensory qualities of fresh-cut iceberg lettuce(Lactuca sativa var, capitata L.) after washing. Journal of Agricultural and FoodChemistry, 57(10), 4195e4203.

Vandekinderen, I., Van Camp, J., Devlieghere, F., Veramme, K., Denon, Q., Ragaert, P.,et al. (2008). Effect of decontamination agents on the microbial population,

J.F.B.de São José et al. / Food Control 45 (2014) 36e5050

sensorial quality, and nutrient content of grated carrots (Daucus carota L.).Journal of Agricultural and Food Chemistry, 56(14), 5723e5731.

Velázquez, L. D. C., Barbini, N. B., Escudero, M. E., & Estrada, C. L. (2009). Evaluationof chlorine, benzalkonioum chloride and lactic acid as sanitizers for reducingEscherichia coli O157:H7 and Yersinia enterocolitica on fresh vegetables. FoodControl, 20(3), 262e269.

Vercet, A., Burgos, J., Crelier, S., & Lopez-Buesa, P. (2001). Inactivation of proteasesand lipases by ultrasound. Innovative Food Science & Emerging Technologies, 2(2),139e150.

Vercet, A., Sánchez, C., Burgos, J., Montañés, L., & Buesa, P. L. (2002). The effects ofmanothermosonication on tomato pectin enzymes and tomato paste rheolog-ical properties. Journal of Food Engineering, 53(3), 273e278.

Yang, Z., Cao, S., Cai, Y., & Zheng, Y. (2011). Combination of salicylic acid andultrasound to control postharvest blue mould caused by Penicillium expansumin peach fruit. Innovative Food Science and Emerging Technologies, 12(3), 310e314.

Zenker, M., Heinz, V., & Knorr, D. (2003). Application of ultrasound assisted thermalprocessing for preservation and quality retention of liquid foods. Journal of FoodProtection, 66(9), 1642e1649.

Zhou, B., Feng, H., & Luo, Y. (2009). Ultrasound enhanced sanitizer efficacy inreduction of Escherichia coli O157: H7 population on spinach leaves. Journal ofFood Science, 74(6), m308em313.