for fresh produce

Kretzschmar, 2009). The economic cost related to food

assessment study conducted by an expert consultationheld in Ann Arbor, USA developed a stepwise approach

studies which demonstrated health concerns associatedwith the chemical residues in green leafy vegetables and

Trends in Food Science & Techvegetables are considered significant carriers of pathogenicmicroorganisms leading to food borne illnesses (Olmez &

(WHO, 2009). This expert group identified key benefitsof using NaOCl apart from a number of laboratories based* Corresponding author.

0924-2244/$ - see front matter 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.tifs.2013.08.008ld

to risk-benefit assessment of chlorine containing disinfec-tants in several food categories including fresh producedetailed. This review identifies the safest disinfectants that

inactive pathogens while maintaining the sensory quality of

fresh produce.

IntroductionThe fresh produce industry continues to be one of the

most important and ever-growing sectors of the globafood market. However, fresh produce such as fruits anKompal Joshia, R. Mahendrana,K. Alagusundarama, T. Nortonb

and B.K. Tiwaric,*aIndian Institute of Crop Processing Technology,

Thanjavur, IndiabDepartment of Engineering, Harper Adams

University, Newport, United KingdomcDepartment of Food Biosciences, Teagasc Food

Research Centre, Dublin, Ireland

(Tel.:D35318059721; e-mails: brijesh.tiwari@teagasc.

ie; brijeshkumartiwari@gmail.com)

Fresh produce such as fruit and vegetables are known car-

riers of pathogenic microorganisms that often lead to out-

breaks of food borne illnesses and public health scares.

During the processing of fresh produce strong sanitizers and

disinfectants are often required to remove the microbiological

load left behind by washing. While such sanitizers and disin-

fectants must be highly efficacious as an anti-microbial agent,

at the same time they must be cost effective, environmentally

friendly, non-hazardous to public health and have insignificant

effect on the nutritional and organoleptic properties of the

fresh produce. This paper reviews the efficacy of various disin-

fectants to reduce the microbial spoilage and to increase the

shelf life of fresh produce without compromising the quality

of the end product. Inactivation of microbes using various dis-

infectants and parameters governing for inactivation areNovel disinfectantsReview

borne illnesses in the United States alone is over 50 billiondollars per year involving more than 48 million peoples(Bermudez-Aguirre & Barbosa-Canovas, 2013). Escheri-chia coli, Salmonella, Shigella spp. and Listeria monocyto-genes are some of the most common microorganismsassociated with such outbreaks (Sapers, 2001). Therefore,cleaning and disinfection is one of the major unit operationsinvolved in the processing of fresh products as it ensuressafety of the products to the consumer. Such operationsshould be carried out without affecting quality and shelflife of the product.

The shelf-life and microbiological quality of fresh pro-duce is largely dependent on washing, cleaning and sani-tizing. Washing of fresh produce in potable water caneffectively remove sand, soil and other debris and tosome extent reduce microbiological load from fresh fruitand vegetables but should not be relied upon to completelyremove microorganisms. Instead, the sanitization or disin-fection agents are required for removal of pathogenic andspoilage microorganisms present on the surface of produceto prevent further spoilage. To achieve the required level ofsanitization or disinfection the chemical used must be ofthe required concentration and applied to the products fora pre-determined time period. The efficacy of these sani-tizers is then based upon their ability to reduce the micro-bial contamination level.

Currently the most widely used chemical disinfectant ischlorine, and it is generally applied in a form of sodium hy-pochloride (NaOCl) in the fresh produce industry. NaOCl isused widely because of its cost effectiveness and efficacy asan antibacterial and antimicrobial agent. An active chlorineconcentration of 5e200 ppm is currently used in the freshproduce industry for disinfection purposes. However, thereaction of chlorine with other organic compounds inperishable produce may lead to the formation of haloge-nated by-products in presence of organic matter givingrise to toxicity concerns. A microbial and chemical risk

nology 34 (2013) 54e61fresh produce. The subsequent report identified an

important gap in the data available on chlorine sanitization,which constrained the scope of risk-benefit assessment(WHO, 2009). This report makes it clear that new sanitizersor technologies to disinfect fruits and vegetables should notonly be highly effective at microbial inactivation but shouldat the same time maintain the sensory quality of the product(Rico, Martin-Diana, Barat, & Barry-Ryan, 2007). Some ofthe novel chemical agents that have gained interest inrecent years include chlorine dioxide, ozone, organic acids,peroxyacetic acid, electrolyzed oxidizing water and

many fruit juices such as apple cider, strawberry and black-berry. Ozone treatment of juices is found to achieve 5 logreduction which is mandatory FDA requirement. Studiesshow that ozone can be employed either in aqueous andgaseous form to achieve desired microbial safety (Cullen,Tiwari, ODonnell, & Muthukumarappan, 2009). Waterflushed with ozone is used for washing of fruits and vege-tables. Minimally processed fruits and vegetables can betreated with aqueous ozone for providing protection againstmicroorganisms. Ozone-containing water was found to

Ozo

11190.572.147.52.1

55K. Joshi et al. / Trends in Food Science & Technology 34 (2013) 54e61hydrogen peroxide. The properties of these disinfectantsare listed in Table 1. The widespread take-up of these sani-tizing agents is due not only to inactivation capabilitiesagainst various pathogenic and spoilage microorganisms(Table 2) but also because their effect on nutritional andorganoleptic properties of fresh produce is trivial. Themain objective of this review is to evaluate novel disinfec-tants that reduce the microbial spoilage of fresh produce.Some applications of novel disinfectant on fresh producediscussed in this review are listed in Table 3.

Chemical disinfectantsOzone

Ozone is tri-atomic oxygen formed by addition ofsinglet oxygen to oxygen molecule. Ozone finds wideapplication in the food industry which mainly concentrateson surface decontamination. Ozone is a powerful antimi-crobial agent that is active against bacteria, fungi, viruses,protozoa, and microbial spores (Khadre & Yousef, 2001;Khadre, Yousef, & Kim, 2001) relevant to fresh produce.Efficacy against both Gram-positive and Gram-negativebacteria and fungi is reported, as well as potential virucidaleffects (Restaino, Frampton, Hemphill, & Palnikar, 1995).Ozone has gained GRAS (Generally Regarded as Safe)for usage because of its property of leaving no residue infood as it is highly unstable and decomposes into oxygenwithout leaving any residue in food product. Ozone is high-ly unstable in aqueous as well as gaseous form as it rapidlydegrades to form hydroxyl (HOe), hydroperoxy (HO2)and superoxide radicals (O2

). These radicals have highoxidizing power leading to the oxidation of vital cellularcomponents. Ozone acts on the cell membranes which aremade up of phospholipids, lipopolysaccharides; it then en-ters inside the cell and damages the DNA and RNA of cell.Ozone can be used as a direct food additive thus, it finds itsapplication in fruit juice industry. Its use has been tested on

Table 1. Properties of disinfectants.

Parameters Chlorine Chlorine dioxide

Boiling point 34.04 C 11 CMelting point 101.5 C 59 CSolubility in water 0.007 g/ml 8 g/L (at 20 C)Density 3.2 g/L (at 0 C) 2.757 g/LAcidity 11.7 3.0Oxidation potential (eV) 1.36 1.57reduce bacterial content in shredded lettuce, blackberries,grapes, black pepper, broccoli, carrots and tomatoes(Kim, Yousef, & Dave, 1999; Sarig et al., 1996; Tiwari,Muthukumarappan, ODonnell, Cullen, & Rice, 2012). Adelay in the growth of green and blue mould is reportedfor ozone treated citrus fruit (Palou, Smilanick, Crisosto,& Mansour, 2001). Microbial studies typically show a2 log reduction of total counts and significant reductionsin spoilage and potentially pathogenic microorganismscommonly associated with fresh produce.

Gaseous ozone can be used as a disinfectant during onfarm storage of fresh produce. Gaseous ozone is reportedto be effective against microorganism during storage waseffectively found to be used on peas and beans (Naito,Okada, & Sakai, 1988), however change in surface colourof some products such as peaches and carrots is reportedwhen treated with ozone. Ozone during storage is alsofound to eliminate odour and reduce the spoilage causedby microorganisms. Studies have shown that the effect ofozone during storage is variable and depends on the typeof microorganism, characteristics of fresh produce and pre-vailing storage conditions. For example, Forney, Song, Fan,Hildebrand, and Jordan (2003) observed a decay resistancetowards Bacillus cinerea in carrots treated with 1000 nl/lozone for 2 or 4 days, however they did not observe a decayresistance towards Sclerotiorum sclerotiorum. Similarly,Skog and Chu (2001) reported that an ozone concentrationof 0.04 ml/l has the potential to extend the storage life ofbroccoli and cucumbers stored at 3 C as compared to 4 C.

Ozone washing of fruits and vegetables is also reportedto degrade pesticide residues. Wu, Luan, Lan, Hung Lo,and Chan (2007) observed that rinsing at a dissolved ozoneconcentration of 1.4 mg/L for 15 min effectively removes27e34% of residual pesticide from vegetables. Higherdegradation of pesticides residues can be obtained withan increase in ozone concentration but with added effect

ne Peroxyacetic acid H2O2

2 C 107 C 0.43 C2 C 150.2 C0 g/L (at 20 C) Completely soluble Miscible4 g/L (at 0 C) 1.0375 g/ml 1.450 g/cm3 (20 C pure)

8.2 11.751.81 1.8

on end product quality (Ou-Yang, Liu, & Ying, 2004).Ozone also helps in increasing shelf life of fruits likeapples, orange (de Oliveira Silva, Bastos, Wurlitzer, deJesus Barros, & Mangan, 2012) and tomatoes by delayingthe ripening of produce.

The effectiveness of ozone against microorganisms pre-sent in food systems depends on several factors, includingthe amount of ozone applied, the residual ozone in the me-dium, various environmental factors such as medium pH,temperature, humidity and additives (surfactants, sugars,etc.) and the amount of organic matter surrounding the cells(Pascual, Llorca, & Canut, 2007). Ozone has a high poten-tial for producing better quality fresh fruits and vegetables

but specific treatment conditions must be defined for eachproduce. In general there is no well-defined negative impactof ozone on the quality of fresh produce when used in therange of 1e5 ppm. Ozone treatments were reported tohave minor effects on anthocyanin contents in strawberries(Perez, Sanz, Rios, Olias, & Olias, 1999) and blackberries(Barth, Zhou, Mercier, & Payne, 1995). Anthocyanin con-tent in blackberries stored in air and at 0.1 ppm ozone, re-mained stable but fluctuated in the 0.3 ppm ozone treatedsamples during storage. There may be a decrease in the as-corbic acid and anthocyanin contents when a large dose ofozone is applied to ensure microbial load reduction this isdue to the presence of direct oxidative compounds formed

Table 2. Disinfectants effect on microbial inactivation.

Chlorine dioxide Hydrogen peroxide Peracetic acid Ozone Electrolyzed oxidizing water

Bacteria U U U U UFungus e e e U ModerateVirus U U U U USpores U U U UPesticide residue e e e U e

Table 3. Application of disinfectant on food products.

Food product Disinfection technique Dose/Concentration Salient finding/Results

Reference

Lettuce Electrolyzed water 5% NaCl solution electrolyzedfor 10 min and 5 min exposure.

6.6 log CFU/ml after 5 min (Paola et al., 2005)

Fresh cut celery Acidic electrolyzedwater

pH 5.6 for 5 min 2.7e2.9 log CFU/g (Issa-Zacharia et al., 2011)

Spinach Electrolyzed oxidizingwater

Contains 100 ppm of residualchlorine at 25 C for 10 min

4e5 log CFU/g (Guentzel, Liang Lam, Callan,Emmons, & Dunham, 2008)

Shredded carrots Alkaline electrolyzed At 50 C 4 log CFU/g (Olaimat & Holley, 2012)

min

56 K. Joshi et al. / Trends in Food Science & Technology 34 (2013) 54e61water and 1% citricacid

Radish sprouts Ozone 2 ppm

Bean sprouts Ozone 2 ppmCarrots Ozone 80 mg/min for 20 min

Tomatoes Gaseous ozone 5.2 mg/L for 15 min

Shredded lettuce Gaseous ozone 5.2 mg/L for 15 minBaby carrots Gaseous ozone 5.2 mg/L for 15 minStrawberry Chlorine dioxide 5 mg/L ClO2 gas for 10Cantaloupe Chlorine dioxide 5.0 mg l1 ClO2 gasCucumber Chlorine dioxide 100 ppm

Lettuce Chlorine dioxide 100 ppm

Guava Chlorine dioxide 100 ppmApples Chlorine dioxide 100 ppmFresh cut leek Peroxyacetic acid 250 ppmTomato Peroxyacetic acid 50 ppm

Lettuce Peroxyacetic acid 50 ppmFresh cut apple Hydrogen peroxide 20 ml/L

Fresh cutcantaloupes

Hydrogen peroxide 2.5% for 2 min1.5 log reduction (Singla, Ganguli, & Ghosh,2011)

1.8 log CFU/g (Singla et al., 2011)4 log reduction for mesophiles (Bermudez-Aguirre &

Barbosa-Canovas, 2013)2.2 log reduction (Singh, Singh, Bhunia, &

Stroshine, 2002)1.6 log reduction (Singh et al., 2002)2.5 log reduction (Singh et al., 2002)4.3e4.7 log reduction (Mahmoud et al., 2008)3.6 log reduction (Mahmoud et al., 2008)3.89 log CFU/g bacterial count (Chung, Huang, Yu, Shen,

& Chen, 2011)3.08 log CFU/g bacterial count (Chung et al., 2011)

4.78 log CFU/g bacterial count (Chung et al., 2011)4 log CFU/g bacterial count (Chung et al., 2011)1.4 log CFU/g (Olaimat & Holley, 2012)4.5 log CFU/g (Keeratipibul, Phewpan, &

Lursinsap, 2011)2.5 log CFU/g (Keeratipibul et al., 2011)>4 log CFU/g (Abadias, Alegre, Usall,

Torres, & Vi~nas, 2011)2.6 log CFU/g bacterial (Olaimat & Holley, 2012)

57K. Joshi et al. / Trends in Food Science & Technology 34 (2013) 54e61as a result of ozone decomposition, these include OH,HO2, O2

, and O3. Formation and stability of these

oxidative species largely depends on storage conditions.

Chlorine dioxideChlorine dioxide (ClO2) exists as a gas at normal tem-

perature (25e30 C) and atmospheric pressure. Chlorinedioxide has been reported for washing of fruits and vegeta-bles and is considered as a processing aid. Like ozone, it isanother powerful oxidizing agent. One of the appreciablephysical properties of ClO2 is that it remains soluble in wa-ter and does not get hydrolyzed. It can be produced via twodifferent reactions: 1) reacting an acid with sodium chlo-rite, or 2) reacting sodium chlorite with chlorine gas(Olmez & Kretzschmar, 2009). Chlorine dioxide possessesstrong bactericide and virucide properties at low concentra-tions of 0.1 ppm (http://www.safeox.com/chlorine-dioxide-clo2). With minimal contact time, it is highly effectiveagainst many pathogenic organisms including bacterialspores, Legionella, Tuberculosis, Listeria, Salmonella,amoebal cysts, Giardia cysts, E. coli, and Cryptosporidium.Importantly, chlorine dioxide is also effective against bio-film hence, bacterial regrowth is significantly retarded.Chlorine dioxide penetrates the cell wall of microorganismsand inhibits metabolic function. It is more efficient thanother oxidizing agent such as chlorine that just burn the sur-face of whatever they come in contact with. Unlike ozoneClO2 is very stable compound. Chlorine dioxide is moreeffective as it can work on range of pH making it more ver-satile. It has limited reactions with the water as it remainsas a true gas when dissolved in water, thus making it effec-tive over wide pH range produce unlike chlorine. Compar-atively ClO2 is highly stable and less corrosive than ozoneand chlorine. It can also remove the unwanted tasteand odour associated with food products. Chlorinedioxide is also reported to reduce microbial populationsin dump tank and wash water (Sapers, 2001). As a disinfec-tant, the use of ClO2 in wash water cucumbers resultedin less than a 90% population reduction on productsurfaces (Sapers, 2001). Chlorine dioxide vapour phasedisinfection of cut green pepper, inoculated with E. coliO157:H7, showed to achieve about 6.45 log unit populationreduction (Sapers, 2001). Sy, Murray, Harrison, andBeuchat (2005) tested the efficacy of gaseous chlorinedioxide at 4.1 ppm to reduce Salmonella on differenttypes of fresh produce. Reductions resulting from thistreatment were 3.13e4.42 log CFU/g for fresh-cutcabbage, 5.15e5.88 log CFU/g for fresh-cut carrots,1.53e1.58 log CFU/g for fresh-cut lettuce, 4.21 log CFU/apple, 4.33 log CFU/tomato, 1.94 log CFU/onion, and3.23 log CFU/peach. Chlorine dioxide gas (ClO2) is a noveland effective method for minimizing pathogens on freshproduce without producing potentially harmful carcino-genic compounds (Rodgers, Cash, Siddiq, & Ryser,2004). Washing of apples showed a 5.5 log CFU reductionof L. monocytogenes on apple skin by treatment with4.0 mg l1 ClO2 gas for 10 min. Additionally, more thana 5 log reduction of E. coli O157:H7 on apple skin wasachieved by treatment with 7.2 mg l1 ClO2 gas for10 min (Mahmoud, Vaidya, Corvalan, & Linton, 2008). Ithas been found that the degree of inactivation by chlorinedioxide increases as pH increases. However, an earlierstudy found that the bactericidal activity of chlorine dioxidewas not affected by pH values in the range of 6.0e10.0(Ridenour & Ingols, 1947). Similar to chlorine, the disin-fection efficiency of chlorine dioxide decreases with adecrease in temperature (Ridenour & Ingols, 1947). Themain drawback of ClO2 is that maximum concentrationof 3 ppm only can be used for whole fresh produce. More-over, the US Code of Federal Regulations necessitates thatthe produce should be rinsed with potable water after ClO2treatment. However, higher dose of chlorine dioxide causesdeterioration of visual quality. For example, prolongedwashing at higher concentration causes darkening (Du,Fu, & Wang, 2009). This could be due to the oxidation ac-tion of ClO2 on phytochemical responsible for colour offruit and vegetables. Adverse changes have also been re-ported in the sensory quality of lettuce on the 3rd day ofstorage after the treatment with 1.4 mg/L chlorine dioxidefor 10.5 min (Tirpanalan, Zunabovic, Domig, & Kneifel,2011).

Hydrogen peroxideHydrogen peroxide is a colourless gas at room tempera-

ture because of its high oxidation potential, it has a highbacteriostatic and bactericidal properties. It has gained in-terest as a potential disinfectant in the fresh produce indus-try because of its strong oxidizing power. It does not reactwith the organic compounds present in perishables to pro-duce carcinogenic compounds and breaks down into waterand oxygen (2H2O2/ 2H2O O2). It has been given thestatus of Generally Regarded as Safe (GRAS) in 1986 forsome of the food commodities. However, hydrogenperoxide causes detrimental quality changes in some foodcommodities for example; it causes browning of appleskin and mushrooms at temperatures greater than 60 C.However, it can be overcome by adding anti-browningagents such as ascorbic acid. It also causes oxidation of an-thocyanins in berries (Sapers, 2001; Sapers & Simmons,1998). Hydrogen peroxide is an effective disinfectantbecause of its efficacy over wide range of pH (6e10). How-ever, it decomposes at pH values greater than 10 (Lee, Park,& Oloman, 2000). Dilute hydrogen peroxide solutions areshown to be effective in reducing microbial load duringwashing of mushrooms apples, and cantaloupes, controllingpostharvest decay of vegetables, thus extending the shelflife of fresh cut vegetables. Hydrogen peroxide concentra-tion of 5% is shown to achieve 3 log unit reduction orhigher when immersed in H2O2 containing water withvigorous agitation at a temperature of 50e60 C for applesand 70e80 C for cantaloupe (Sapers, Miller, Pilizota, &Mattrazzo, 2001; Sapers & Simmons, 1998). Application

58 K. Joshi et al. / Trends in Food Science & Technology 34 (2013) 54e61of high temperature and hydrogen peroxide can achieveabout 2 log reduction for E. coli and Salmonella. However,low concentration of H2O2 (1%) is considered to be ineffec-tive against disinfection of cantaloupes at low temperatureof 20 C for 15 min for E coli and Salmonella. In the samestudy, 1% hydrogen peroxide at 20 or 40 C for 15 minreduced E. coli O157:H7 numbers by 1.8e3.5 log CFU/gon intact apples. Disinfection by using hydrogen peroxidehave also been effective in reducing pathogen micro-organisms on whole grapes, prunes, oranges, mushrooms,melons, tomatoes, red bell peppers, lettuce, cucumbers,zucchini and bell peppers (Rico et al., 2007). H2O2 isalso reported to reduce poly phenol oxidase (PPO) enzymeactivity in Chinese water chestnut (Peng, Yang, Li, Jiang, &Joyce, 2008). The dipping treatment in the solution of H2O2resulted in severely browning of some of the products(shredded lettuce, berries, mushroom). Thus, it is notpreferred to decontaminate such produce. The main prob-lem associated with the use of hydrogen peroxide is thatwhen shredded lettuce is dipped in it for long time brown-ing takes place thus it is not suitable for processing greenleafy vegetables (Parish et al., 2003).

Peroxyacetic acidPeroxyacetic acid also known as peracetic acid (PA) is

actually an equilibrium mixture of the peroxy compound,hydrogen peroxide, and acetic acid. It has been recommen-ded for treatment of process water. Like ozone and chlo-rine dioxide, peroxyacetic acid is effective in theinactivation of pathogenic microorganisms such as E.coli, Salmonella, Listeria in suspension at lower concentra-tions compared to chlorine. It is also known to be effectiveagainst viruses and microbial spores. PA is gainingincreased interest as an alternative to chlorine disinfectantsbecause it does not produce harmful by products and de-composes into acetic acid, water and oxygen (Olmez &Kretzschmar, 2009). Peracetic acid has been reported foruse in dairy, cheese processing plants, on food processingequipment, and as disinfectant in breweries, wineries, andbeverage plants. Efficacy of peracetic acid is influenced bypH and temperature however, it is reported to be uninflu-enced by the presence of other organic compounds in thewater. Peracetic acid is more effective at neutral pH of 7and efficacy reduces at higher pH values. Higher tempera-ture and neutral pH acts as synergistic for microbial inac-tivation for example at 15 C and 7 pH, the efficacy ofperacetic acid is almost one fifth compared to activity at53 C and 7 pH. Efficacy of PA is very similar to other dis-infections discussed. PA disinfects by oxidizing of theouter cell membrane of vegetative bacterial cells, endo-spores, yeast, and mould spores. The mechanism of oxida-tion is the transfer of electrons, therefore the stronger theoxidizer, the faster electrons are transferred to the microor-ganism and the faster the microorganism is inactivated(NOSB TAP Materials Database complied by OMRI).The US Code of Federal Regulations states that the useof peroxyacetic acid in fruits and vegetables is allowedup to 80 ppm in water used for washing. The microbial re-ductions for aerobic bacteria, coli forms, yeasts andmoulds on fresh-cut celery, cabbage and potatoes at80 ppm peroxyacetic acid, were less than 1.5 log units(Forney, Rij, Denis-Arrue, & Smilanick, 1991). Sapers(2001) obtained a 2 log units reduction in apples inocu-lated with E. coli O157:H7 using 80 ppm peroxyaceticacid, but the interval between inoculation and treatmentwas only 30 min. In contrast, in a similar apple study,Sapers (2001) obtained less than a 1 log unit reduction atperacetic acid concentration of 80 ppm, at after 24 h of mi-crobial inoculation. In order to exceed the apparent popu-lation reduction of 1e2 log units, more effective sanitizingagents and application methods must be used that providesbetter contact between the sanitizing agent and microbialattachment sites on produce surfaces.

Electrolyzed oxidizing waterElectrolyzed oxidizing water (EOW) is ionized water.

EOW water can be produced by passing a salt solution(12%) across a bipolar membrane, resulting in two solu-tions: an acidic solution that is characterized by a lowpH, high Oxidation Reduction Potential (ORP). The othersolution is basic and composed of a high pH and lowORP. The sodium ions are drawn to the cathode (NaOH)and the chlorine ions are drawn to the anode (HOCl). Thealkaline EO water so collected has a pH of approximately11.4 and ORP of 795 mV, while acidic EO water has apH of approximately 2.6, ORP of 1150 mV and a chlorineconcentration of 40e90 ppm. Recently the use of EOWas asanitizing agent for fresh produce has received lot of atten-tion for microbial load reduction purposes.

The mechanism of EOW can be explained in three mainsteps i.e. electrolysis restructures water, electrolysischanges the oxidative reduction potential (ORP), changesthe pH. Restructuring of water refers to breakdown oflarger size molecules into smaller size so that it can effi-ciently penetrate the cell wall of microorganisms on freshproduce. The resulting acidic water lacks electrons thuscalled oxidizing water and has a sufficiently high ORP,which results in the inactivation of pathogenic microorgan-isms by depriving microorganisms of electrons. In case ofalkaline water it is rich in electrons thus known as reducingwater. It has ability to neutralize free radicals efficientlythus acting as an excellent antioxidant.

Acidic Electrolyzed Water (AEW) and Neutral Electro-lyzed Water (NEW) are two forms of EOW and these solu-tions are generated by electrolysis of a dilute NaCl solutionpassing through the anode of a membrane electrolyser.AEW has a strong bactericidal effect on most of pathogenicbacteria due to its low pH (2e4), high oxidation reductionpotential (ORP > 1000 mV) and the presence of active ox-idizers like hypochlorous acid. In general NEW is similar toAEW, but a part of the product formed at the anode is re-directed into the cathode chamber, thus increasing the

59K. Joshi et al. / Trends in Food Science & Technology 34 (2013) 54e61content of ClO ions. Because of its neutral pH, NEW doesnot contribute as aggressively as AEW to the corrosion ofprocessing equipment or irritation of hands, and is morestable because chlorine loss is significantly reduced at pHrange of 6e9 (Hsu & Kao, 2004; Len et al., 2002). Izumi(1999) has evaluated the effect of Neutral Electrolyzed Wa-ter (pH 6.8 and 20 mg/L active chlorine) on total microbialcount in fresh-cut vegetables. Izumi (1999) also reported E.coli or Salmonella reduction of up to 2.6 log CFU g/L witha non significant effect on plant tissue pH, surface colourand general appearance of vegetables such as bell pepper,spinach and fresh cut carrots. The advantage of EOW forthe inactivation of pathogenic microorganisms relies onits less adverse impact on the environment as well as usershealth because of no residues and by-products as a result ofdisinfection.

Electrolyzed oxidizing water (EOW) has been reportedto have strong bactericidal effects on E. coli O157:H7, L.monocytogenes, Bacillus cereus, and Salmonella species.In addition, it could disinfect hepatitis B virus and humanimmunodeficiency virus (HIV) (Hati et al., 2012) andreduce germinations of many fungal species (Buck, VanIersel, Oetting, & Hung, 2002). Acidic EO water wasused to treat fresh cut vegetables, and results achieved upto a 2.6 log10 CFU/g reduction in bacterial population.Sapers (2001) reported population reductions of E. coliO157:H7 on apples of 3.7e4.6 log units. EOW was foundto be effective in reducing E. coli O157:H7 and L. monocy-togenes population by 2.41 and 2.65 log by washing lettucewith EOW (45 mg/L free chlorine), agitated at 100 rpm for3 min compared to H2O2 treatment under similar condi-tions. The result also highlighted that EOW treatment didnot significantly affect the quality characteristics such ascolour and general appearance of lettuce (Issa-Zacharia,Kamitani, Miwa, Muhimbula, & Iwasaki, 2011). Similarly,the quality changes in fresh produce by AEW washing areminimal or insignificant compared to chlorine wash (Gopal,Coventry, Wan, Roginski, & Ajlouni, 2010). However,some browning of lettuce is reported in some cases howev-er there is no adverse effect on the sensory quality of theproduce (Tirpanalan et al., 2011). Electrolyzed alkaline wa-ter contains a small amount of sodium hydroxide which is amaterial of soap, and is effective in washing away proteins,fats and oils which are difficult to remove by water (Huang,Hung, Hsu, Huang, & Hwang, 2008).

Combinations of chemical disinfectantsHurdle technology which means combination of

different methods for preservation is often employed formicrobial safety of fresh produce (Rico et al., 2007).The combination of various sanitizing agents is regularlyused to increase the efficacy of disinfectant against micro-bial population reduction. Combined treatments are advan-tageous because many individual treatments alone are notadequate to ensure food safety or stability. Electrolyzedoxidizing water has significant enhanced sanitizationcapability when it is used in combination with variouschemicals. Paola, Roco, and Marcela (2005) observedthat EO water when combined with 0.6% of acetic acidshowed higher reduction of 5.49 log CFU/g on lettuce.Essential oils like thyme oil and lemongrass oil are a prom-ising method for disinfecting but very high concentration isrequired when used for fresh produce for disinfection (Abd-AllA, Abd-El-Kader, Abd-El-Kareem, & El-Mohamedy,2011). However combination of these essential oils withother chemicals or EOW can turn out to be promising alter-native for disinfection. Studies showed that when lettucewas treated with 0.6% acetic acid after EO water treatment,there was a higher reduction in cell population(5.49 log CFU/g). Sonication of ozonized water has provedto be an excellent method for sanitizing as its kills all mi-croorganisms along with removing the surface pesticideresidue (Tirpanalan et al., 2011). Williams, Sumner, andGolden (2005) reported that combinations of hydrogenperoxide and ozone treatment followed by refrigerated stor-age caused greater than 5 log CFU/ml reduction of E. coliO157:H7 and Salmonella in apple cider and orange juice.Some of the natural antimicrobial agents such as plant ex-tracts (phytoalexins), bacteriocins, and organic acids canalso be used along with it to increase the efficiency andreduce the risk of carcinogenic compounds. Some of theother hurdles which are used are temperature, water activitywhich can be tailored properly with existing process tomake it more efficient.

The efficacy of ozonation may be increased by use incombination with other technologies. The disaggregatingeffect of ultrasound upon solid matter and on gas bubblesmay improve efficacy by increasing surface area availablefor the sanitation to occur. Furthermore, ultrasound accel-erates the sedimentation of oxidizing organic matter, thusreducing ozone demand. Williams et al. (2005) reportedthat combinations of hydrogen peroxide and ozone treat-ment followed by refrigerated storage causes greater than5-log CFU/ml reduction of E. coli O157:H7 and Salmo-nella in apple cider and orange juice. Some microorgan-isms are sensitive to lower concentrations of oxidizingagents when exposed to ultrasound, and the combined ac-tion of UV radiation with high frequency ultrasound in-creases the rate of bacterial inactivation (Sierra &Boucher, 1971). Employing such hybrid techniques canalso reduce the dosage of the chemical disinfectantrequired. Thus by using the combination of sonicationand ozone or hydrodynamic cavitation and ozone, the con-centration of ozone required for disinfection may be signif-icantly reduced to half or one-third depending upon thetype of microorganism (Tiwari et al., 2012). The combina-tion of hydrodynamic cavitation and ozone proved to be anefficient method of water disinfection (Jyoti & Pandit,2004). Yuk, Yoo, Yoon, Marshall, and Oh (2007) foundthat a combined ozone and organic acid treatment wasmore effective than individual application for control ofE. coli O157:H7 on mushrooms.

Conclusion

Disease, 86(3), 278e281.

Guentzel, J. L., Liang Lam, K., Callan, M. A., Emmons, S. A., &

60 K. Joshi et al. / Trends in Food Science & Technology 34 (2013) 54e61Chung, C.-C., Huang, T.-C., Yu, C.-H., Shen, F.-Y., & Chen, H.-H.(2011). Bactericidal effects of fresh-cut vegetables and fruits aftersubsequent washing with chlorine dioxide. In Proceedings ofinternational conference on food engineering and biotechnology(ICFEB 2011).

Cullen, P. J., Tiwari, B. K., ODonnell, C. P., & Muthukumarappan, K.(2009). Modelling approaches to ozone processing of liquid foods.Trends in Food Science & Technology, 20(3e4), 125e136.

Du, J., Fu, Y., & Wang, N. (2009). Effects of aqueous chlorine dioxidetreatment on browning of fresh-cut lotus root. LWT e FoodScience and Technology, 42(2), 654e659.

Forney, C. F., Rij, R. E., Denis-Arrue, R., & Smilanick, J. L. (1991).Vapor-phase hydrogenperoxide inhibits postharvest decay of tablegrapes. HortScience, 26, 1512e1514.

Forney, C. F., Song, J., Fan, L., Hildebrand, P. D., & Jordan, M. A.(2003). Ozone and 1-methylcyclopropene alter the postharvestquality of broccoli. Journal of the American Society forHorticultural Science, 128(3), 403e408.

Gopal, A., Coventry, J., Wan, J., Roginski, H., & Ajlouni, S. (2010).Alternative disinfection techniques to extend the shelf life ofminimally processed iceberg lettuce. Food Microbiology, 27(2),210e219.Recently it has been observed that there is a shift in thediet of human beings to fresh fruits and vegetables. Fruitand vegetables must at least undergo minimal processingto guarantee produce that is safe and of high quality. It ishighly important that the produce is free from microbialcontamination with minimum with no deleterious effecton the quality of the fresh produce. Chlorine, the mostcommonly used disinfectant, has serious health hazardsleading to formation of carcinogenic compounds in pro-duce. Some other novel and efficient disinfectants usedfor decontamination include chlorine dioxide, ozone,hydrogen peroxide, per acetic acid/peroxyacetic acid, elec-trolyzed oxidizing water. This paper demonstrated thatthese are safe for usage and does not leave any residuebehind. Moreover, the paper showed that there is a newemerging trend in industry which is the hurdle technologyor combination of different chemicals with capabilities toachieve higher levels of safety in fresh produce.

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Novel disinfectants for fresh produceIntroductionChemical disinfectantsOzoneChlorine dioxideHydrogen peroxidePeroxyacetic acidElectrolyzed oxidizing water

Combinations of chemical disinfectantsConclusionReferences