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Said the researchers, “by measuring theabsorbency at 1 min, we have demonstrated that accuracy could besubstantially improved.” The results were published in “Underesti-mation of Pyruvic

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Industrial Applications of Selected JFS Articles

We are seeing just how important flavor compounds are—the

amount of pungency in onions, the characterization of flavor in

certain kinds of honey As standardization of flavor becomes key,

products can even be in trouble for tasting better than they should!

Instrumentation helps—the human tongue and nose is the final

judge, but numbers can help More papers are appearing with

work on nanotechnology, as well; an understanding of how this

new science works is imperative to the up-to-snuff technologist

(and engineer and marketer)

Learning a Little More about Nanoemulsion Phases

A paper titled “Optimization ofβ-Casein Stabilized

Nanoemul-sions Using Experimental Mixture Design” outlines the changes

in viscosity and glass transition temperature that exists in the

con-tinuous phase of nanoemulsion systems, and how those attributes

affected stability of a product Emulsions were made that included

β-casein at 4 levels, lactose and trehalose at several levels Higher

levels ofβ-casein content resulted in increased viscosity and

de-creases in melting temperatures A mixture design was used to

predict the optimum levels of lactose and trehalose needed to

reach minimum and maximum Tg and viscosity in solution at

fixed protein contents C1108–1117

Keeping Probiotics Useful

Freeze-drying probiotics and storing the dried powder, the usual

way to process the probiotics for commercial use, appears to reduce

the viability of the materials A group of researchers are looking

into the efficacy of using a glassy state for the little varmints, and

retaining the glassy state during drying In “Role of Glassy State

on Stabilities of Freeze-Dried Probiotics” the authors describe the

glassy state that should be retained during freezing, drying, and

storage of cells Insight into the role of glassy state has been largely

adopted from studies conducted with proteins and foods, especially

sugars Say the researchers, “Current understanding of the role of

the glassy state on viability of probiotics is not only valuable for

the production of fermented foods and nutraceuticals but also

for the development of nonfermented functional foods that use

the dried powder as an adjunct.” The paper, a review of recent

findings regarding glassy states and the effects on probiotic survival,

notes that 1000 articles and reviews were published in 2008, and

more information is appearing, supporting the introduction of $16

billion in the U.S alone in 2008 R152–156

How Pungent Is that Onion?

In determining how pungent an onion is, one standard reacts

onion juice with 2,4-dinitrophenylhydrazine (DNPH) It’s been a

standard test since 1961, measuring the pyruvic acid concentration

in onion juice However, researchers found that the absorbency ofthe color adduct of the reaction dropped fast, as compared to that

of the pyruvic acid standards, which meant that the pyruvic acidwas higher than estimated Said the researchers, “by measuring theabsorbency at 1 min, we have demonstrated that accuracy could besubstantially improved.” The results were published in “Underesti-mation of Pyruvic Acid Concentrations by Fructose and Cysteine

in 2,4-Dinitrophenylhydrazine-Mediated Onion Pungency Test.”Alliinase action in juice (fresh or cooked) and bulb colors did notaffect the degradation Some organic acids indigenously found inonion, such as ascorbic acid, proline, and glutamic acid, did not re-duce the absorbency However, fructose within the onion juice orsupplemented caused the degradation of the color adduct, whereassucrose and glucose also affected the test, but had a lesser effect.Degradation rates increased proportionally as fructose concentra-tions increased up to 70 mg/mL Cysteine was found to degradethe pyruvic acid itself before the pyruvic acid could react withDNPH This happened rapidly So if the degree of pungency ofonion ingredients is important to control, this study is important

C1136–1142

Films for Packaging Are Built with Agar, Special Clays

Water vapor adsorption behaviors are changed in nanofilmsmade from agar and nanoclay according to the type of nanoclaysused In the paper titled “Water Vapor Adsorption Isotherms ofAgar-Based Nanocomposite Films”, the author discusses methodsused to get an understanding of the effects of various nanoclays:The Guggenheim–Anderson–de Boer (GAB) isotherm model pa-rameters were estimated by using both polynomial regression andnonlinear regression methods, and the behavior of the nanocom-posite films was found to be greatly influenced by the type ofclay It was found that the GAB model fitted adequately for de-scribing experimental adsorption isotherm data for the film sam-

ples The monolayer moisture content (mo) of the film samples

was also greatly affected by the type of nanoclay used, that is,

mo of nanocomposite films was significantly lower than that of

the neat agar film For background information, for those notinto nanotechnology, bionanocomposites are hybrid materials ofbiopolymer with inorganic fillers which have at least one dimen-sion in the nanometer scale It is generally known that nanoscaledispersion of the filler phase in the polymer matrix leads to prop-erty enhancements such as decreased permeability to gases (O2,

CO2, and water vapor) and liquids, better resistance to solvents,increased thermal stability, and improved mechanical properties

N68–72

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Speaking of Word Count .

About a year ago, we informed the potential authors of future

manuscripts submitted to sections of the Journal of Food Science

that we would be limiting word count on manuscripts In this

action, we were trying to decrease the number of printed pages

particularly for JFS while enhancing the readability of the papers.

In a survey of printed papers at that time, Amanda Ferguson

discovered that most manuscripts to JFS were a little over 5,000

in word count, and manuscripts in Comprehensive Reviews in Food

Science and Food Safety were all over 10,000 words With those data

as the guideline, we set a JFS research manuscript word count limit

(excluding tables and figures) at 5,000 words and minimum word

count for CRFSFS at 10,000 words Starting November 2011,

au-thors were asked to voluntarily submit word count on manuscripts

and in January 2011, words count was required Needless to say,

we had some flexibility in applying the word count rule On the

other hand, I received not one letter to the editor decrying the

use of word count or complaining that it was too limiting Nor

did I receive any oral argument while I attended the IFT AMFE

in June I take this inaction as a sign of not only acceptance but of

support for word count limitation

With that in mind, I asked Amanda to again do a survey of word

count on our accepted manuscripts The data for a sampling of

papers published in 2011 are in and they tell the following story

JFS-Concise Reviews Avg. 7893.67 5266-12606

JFS-Research Sections Avg. 4544.28 1930-8454

Of the 141 papers in the JFS research sections, only 18 wereover the 5,000 word limit, and only 3 were more than 1000 words

over The mean of 4500 word count for the research sections of JFS

compares to the October 2010 reported mean of 5140 and range

of 2350-8560 Only 1 review paper in JFS was over the 10,000

word limit The effect of the decrease in word count was to duce the page count per paper from 7.3 to 7.0 In other words, thechange achieved the result we were hoping for and there were notuntoward consequences Now, for the kicker, should we be look-ing at a 4,500 word count limit for research papers submitted to

re-JFS for 2012? Send your thoughts to me at dlund@cals.wisc.edu.

Daryl LundEditor in Chief

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Chalat Santivarangkna, Mathias Aschenbrenner, Ulrich Kulozik, and Petra Foerst

Abstract: High viability of dried probiotics is of great importance for immediate recovery of activity in fermented foodsand for health-promoting effects of nutraceuticals The conventional process for the production of dried probiotics isfreeze-drying However, loss of viability occurs during the drying and storage of the dried powder It is believed thatachieving the “glassy state” is necessary for survival, and the glassy state should be retained during freezing, drying, andstorage of cells Insight into the role of glassy state has been largely adopted from studies conducted with proteins andfoods However, studies on the role of glassy state particularly with probiotic cells are on the increase, and both commonand explicit findings have been reported Current understanding of the role of the glassy state on viability of probiotics isnot only valuable for the production of fermented foods and nutraceuticals but also for the development of nonfermentedfunctional foods that use the dried powder as an adjunct Therefore, the aim of this review is to bring together recentfindings on the role of glassy state on survival of probiotics during each step of production and storage The prevailing state

of knowledge and recent finding are discussed The major gaps of knowledge have been identified and the perspective ofongoing and future research is addressed

Keywords: freeze drying, glass transition, lactic acid bacteria, probiotics

Introduction

Research and interest regarding probiotics is receiving more

focus than ever before For example, in 2008, more than

1000 articles and reviews were published on the subject and more

than 2000 probiotic products launched (Jankovic and others 2010)

The global market for probiotic products was worth US$16 billion

in 2008, and the estimated target is a total of US$19.6 billion in

sales in 2013 (Granato and others 2010) For food applications,

probiotics are mainly employed alone or together with starter

cultures in fermented dairy products (for example, yogurts and

cultured drinks) In addition, probiotics are also potentially used

as nutraceuticals and dry adjunct in nonfermented and nondairy

products, such as fruit juices, cereals, dried powder foods

(Rivera-Espinoza and Gallardo-Navarro 2010) In either case, high

vi-ability of probiotics is of great importance in order to ensure

immediate recovery of fermentation activity (especially Direct Vat

Inoculation-DVI cultures) and to meet the minimal requirements

for health-promoting effects

The standard process for the production of dry probiotics is

freeze-drying The typical freeze-drying process consists of 3 steps:

freezing, primary drying, and secondary drying During these

3 steps, cells are exposed to various stresses, especially

dehydra-tion, compromising cell survival A further survival reduction

oc-curs during storage of the dried powder, where the key storage

conditions such as relative humidity and temperature play a major

role In addition to physiological states of cells, the physical state

of the surrounding sample matrix is believed to be critical for

sur-vival of probiotics The high viscosity of a surrounding amorphous

MS 20110302 Submitted 3/9/2011, Accepted 6/21/2011 Authors are with Chair

for Food Process Engineering and Dairy Technology, Centre of Life and Food Sciences,

Technische Univ M¨unchen, 85354-Freising, Germany Direct inquiries to author

Foerst (E-mail: petra.foerst@wzw.tum.de).

glass can inhibit diffusion and slow down deleterious reactions orchanges in the structures and chemical composition The role

of glassy state on the functionalities, bioactivity, and stability ofenzymes, pharmaceutical proteins, and foods has been widely re-ported Nevertheless, current studies on the role of glassy state,particularly with probiotics, are on the increase and both com-mon and explicit findings have been found It is an aim of thisreview to bring together recent findings on the role of glassy state

on survival of probiotics during each step of the production and

of the storage period The prevailing state of knowledge related tothe role is revisited, and recent finding is discussed

Glassy State

The glassy state is referred to an amorphous metastable statethat resembles a solid but without any long-range lattice order,that is, the position of molecules relative to another is more ran-dom In other words, it has a solid characteristic/appearance but amolecular arrangement that is more typical for liquids A glass has

an extremely high viscosity (for example, typically≥ 1012 Pa s)and shows temperature-dependent transition (Slade and Levine1991) When a glass is heated above a certain temperature, themolecules gain translational mobility and enter a liquid-like state.The transformation of solid- to liquid-like state is known as glasstransition The most common parameter describing the glassy state

and its transition is the glass transition temperature (T g or T gfor

a maximally freeze-concentrated solution), below which

mate-rials exhibit the extremely high viscosity At T < T g, diffusionlimited deterioration reactions are inhibited because water in theamorphous glass is immobilized and unavailable

In various studies, sugars or strong glass-forming polymers have

been added in an effort to increase T g of dried probiotics This

is based on the observation that many anhydrobiotes accumulatelarge amount of sugars, especially trehalose and sucrose, inside thecells, for example, 25% of DW (Buitink and Leprince 2004) The

C

r Vol 76, Nr 8, 2011

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presence of sugars on both sides of the cells was considered being

necessary for protection against freezing (Duong and others 2006)

and dehydration (Tymczyszyn and others 2007) Crowe and others

(1987) found that intra- and extracellular sugars provide protection

of proteins and membranes by forming a glassy matrix that is able

to interact via hydrogen bonding This protective effect of sugars

on biomolecules was reported to appear only in case of

amor-phous carbohydrate glasses, but not in case of crystalline sugars

(Pikal and Rigsbee 1997; Izutsu and Kojima 2002) In contrast to

the drying of pharmaceutically relevant proteins, where the

sensi-tive biomolecules are directly embedded in the amorphous sugar

glass, several drying-sensitive components of bacterial cells are

sit-uated in the intracellular space Therefore, the protectant must be

transported through the cell membrane Thus, many high

molec-ular weight (MW) polymers that show limited transportation into

cells or in penetration and interaction with the phospholipid

head-groups of the cell membrane are not very effective in protecting

dried probiotics (Semyonov and others 2010)

According to Potts (1994), it is still not clear if bacterial glasses

exist The differential scanning calorimetry (DSC) technique

which is commonly used for the detection of glass transition,

is insensitive for cells, where changes in heat capacity are small and

or when many transitions occur in the same temperature range

For example, Fonseca and others (2001) showed that the T g of

washed cells of Lactobacillus bulgaricus cannot be detected

Further-more, Cerrutti and others (2000) and Fonseca and others (2001)

indicated that the reported T gis mainly obtained from the added

solutes or the drying matrix However, Hoekstra and others (2001)

and Sun and Leopold (1997) showed that the state of the cytoplasm

is considered to be of crucial importance for the dehydration

tol-erance in organisms Thus, the glassy state of dried cells (if there

is any) needs to be considered carefully

Role of Glassy State during Freezing

The typical freeze-drying or lyophilization process consists of

3 steps: freezing, primary drying or sublimation, and secondary

drying or desorption The ice crystals formed during freezing

determine the morphology and distribution of the pores

(macro-scopic cake structure) that are formed during the removal of ice

crystals Thus, the freezing process significantly determines the

drying behavior of the sample throughout the following process

steps In order to ensure rapid drying and to facilitate vapor

migra-tion during drying, ice crystals in the suspension should be large

and contiguous On the one hand, large ice crystals can only be

achieved by relatively slow freezing rates (not with liq N2) On

the other hand, these large ice crystals can induce cell damage

due to mechanical stress Generally, slow freezing may accompany

the eutectic crystallization of buffer salt components, which is also

suspected to cause membrane damage (Morgan and others 2006)

In other words, optimum freezing conditions often require a

com-promise between the requirements of the bacteria and the drying

performance For the production of probiotics, frozen granules are

commonly produced by distributing the cell suspension through

a droplet disc with pores or through a nozzle into liquid N2 In

addition to direct freezing in liquid N2, innovative rapid freezing

methods were explored by Volkert and others (2008) The frozen

granules are produced by the spray freezing, where cell suspension

is sprayed in an air blast freezer to get droplets (for example, size of

ca 5 to 30μm) For a frozen solution, at T g,the high viscosity of

the unfrozen phase will inhibit ice crystal formation; and therefore,

a maximally freeze-concentrated solution is formed (Roos 1997)

It has been suggested that the formation of a maximally

freeze-concentrated matrix with entrapped microbial cells is essential forthe survival during freezing (Pehkonen and others 2008) Given

T gof skim milk (–50C), sucrose (–46C), and trehalose (–40C),

which are the most common suspending medium used in many

studies, and T gof pure water (–135C), the maximally

freeze-concentrated matrix should be obtained by common industrialfreezing protocols, for example, immersion in liquid N2(–196C)

Otherwise, the freezing temperature should be selected with care

to ensure a maximally freeze-concentrated state and formation of

a glassy structure of the unfrozen continuous phase of the cell pension In freeze-drying formulations, cryoprotectants are used

sus-to forestall cell injury Some viscous cryo-protectants (for example,glycerol, sugars, and polymers) increase the viscosity of the freeze-concentrated solution or cytoplasm depending on their permeabil-ity Therefore, the glassy state can be reached at a lower coolingrate and a higher freezing temperature (Morris and others 2006)

The annealing step is commonly used for the freeze-drying

of proteins and pharmaceuticals However, it is not applied forthe production of freeze-dried probiotics Annealing is a pro-cess, where frozen samples are kept isothermally at a temperature

between T gand the onset of melting temperature During ing, freezable water entrapped in amorphous regions (due to rapidfreezing) is crystallized into larger and more uniform ice crystals

anneal-This is especially true for the frozen probiotics, which are monly produced by rapid freezing using liquid nitrogen A pellet

com-of 2 mm diameter is cooled from 0 to –50C in approximately

10 s or at a freezing rate of approximately 300C/min (Oetjen andHaseley 2003) The increased content and uniform ice formationimprove the efficacy of subsequent drying process The knowledge

of the influence of annealing on probiotics’ survival and stability isvery limited In a study by Ekdawi-Sever and others (2003), it wasreported that the annealing does not cause cell death, but improves

storage stability and reduces browning reaction of L acidophilus.

Role of Glassy State during Drying

It is the current opinion that the product temperature duringremoval of ice crystals should not be higher than the critical tem-

perature This critical temperature commonly refers to T g(or T

g

after sublimation) In this respect, the processing conditions, (forexample, pressure and shelf temperature during sublimation) must

be controlled so that the product temperature is not higher than

T gduring drying For this reason, solutes with high T

gare often

added to increase T g so that the drying can be carried out at a

higher temperature, and a high T gof final dried products is tained to provide a high storage stability Disaccharide sugars andoligomeric sugars are preferred as additives for freeze-drying not

ob-only because they exhibit a higher T g(Adams and Ramsay 1996),but also because they can be easily vitrified (Franks 1998; Ward andothers 1999) For sugar alcohols such as mannitol, caution must

be exercised Mannitol can easily separate from a frozen solution

in the form of a crystalline phase (Adams and Ramsay 1996; Kimand others 1998), resulting in a loss of the product stability afterfreeze-drying (Izutsu and others 1994; Izutsu and Kojima 2002)

This reason has been proposed for the little or no protection ferred by mannitol on freeze-dried malolactic cultures (Zhao andZhang 2005)

con-Recently, “collapse temperature” which is defined as the imum temperature preventing the structure of the dried product

max-from macroscopic collapse (T c) (Fonseca and others 2004a) wasproposed to use as the critical temperature for freeze-drying of

drying formulation with cells In comparison, T c and T gare sured with techniques based on different principles DSC has been

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Glassy state of dried probiotics

commonly used over decades to determine the T g as a mid- or

onset point of the temperature range that the endothermic shift in

heat capacity appears The measurement of T gis carried out with

a representative frozen sample ex situ at atmospheric pressure In

contrast, T cis commonly determined by a freeze-drying

micro-scope as the visual structural collapse during the simulated

subli-mation of ice crystals under a set vacuum level In other words, T c

reflects the physical state of frozen matrix during drying, whereas

T grather reflects the physical state regardless of the drying

condi-tions The state diagram showing glass transition temperature and

collapse temperature is depicted in Figure 1 (adapted and modified

from Roos 2010) In the absence of cells, the difference between

T gand T

cis very small Although the presence of cells does not

clearly influence T g(Fonseca and others 2001; Schoug and

oth-ers 2006), it significantly increases T c(Fonseca and others 2004a)

Bacteria can give some kind of structure and thus reduce or avoid

viscous flow when T g of pure sugar solution is reached The

in-crease depends on the cell types, that is, size, shapes, and cell chain

formation and concentration (Fonseca and others 2004b) As a

re-sult, a freeze-drying matrix with cells is more robust, and when T c

is taken as the critical temperature, it allows the drying stage with

a higher product temperature (or practically drying temperature)

This is of economical importance because it is estimated that the

increase in a degree of product temperature will decrease primary

drying time by about 13% (Tang and Pikal 2004)

Nevertheless, the opinion that cells should be retained in glassy

state during drying lacks clear empirical evidence The physical

state has been measured mostly by analyzing the frozen and dry

sample before and after drying, while the physical state during

drying is changed with drying time and conditions In our

re-cent study (Foerst and others 2010), several drying protocols were

carried out, and the viability was considered in relation to

physi-cal state, residence time in rubbery state and moisture content of

samples The study showed that glassy state may not play a

signif-icant role on viability of cells during drying step of freeze-drying

The survival decreased similarly for conditions where the samples

remained in glassy state for the whole part of drying, and for

con-dition where the difference between product and glass transitiontemperature was so high that the sample showed a collapsed struc-ture The results are in agreement with unexpected results from arecent study by Schersch and others (2010) with pharmaceuticallyrelevant proteins Loss of biological activities of the proteins wasnot observed in collapsed and noncollapsed cakes The collapsedlyophilizate, the appearance of which is unacceptable for pharma-ceutial products, is not critically important for probiotic products.The dried lyophilizate has to be milled into powder to be mixedwith other food components, mixed with other fillers for probi-otic tablets or capsules, as well as used as starter cultures Whenthe collapsed structure as a result of drying does not negatively af-fect the viability of cells, the proposed concept “collapse drying,”which is expected to substantially reduce drying time (Scherschand others 2010) can be possibly applied for the production offreeze-dried probiotics

In addition to free water, which is removed during primarydrying, cells contain ca 0.25 g water/g dry weight of stronglyassociated water that is unfreezable This strongly associated water

is removed by desorption The shelf temperature is elevated topromote desorption of water At the end of the secondary dry-ing, the sample should have a water content that is optimal forstorage It has been suggested that the moisture content of 1%

or less is required for a long-term shelf life (Nakamura 1996);however, Gardiner and others (2000) showed that moisture re-moval below 4% may be considered practically enough It wasalso reported in a study by Zayed and Roos (2004) that the opti-

mal moisture content for storage of freeze-dried L salivarius ssp salivarius is in the range of 2.8% to 5.6% Therefore, it is still

debatable whether cells should be dried to moisture content aslow as possible An argument is that lipid oxidation is enhanced

at very low water contents, and water acts as a protectant againstoxidation

Role of Glassy State during Storage

Low moisture contents of dried cells after drying do not tee high stability during storage The moisture is not constant, and

guaran-Figure 1–State diagram showing different

regions and state of a drying matrix: T m, onset

of ice melting; T m, onset of ice melting in a maximally freeze-concentrated solute matrix;

T g , glass transition temperature; T g, glass transition temperature of the maximally

freeze-concentrated solute matrix; T gw, glass

transition of water, and T c, collapsed

temperature T c approximate to T gand increases in the presence of cells The shaded area shows a temperature range for maximum

ice formation for the solute concentration C g The glass line indicates the glass transition temperature at various solute concentrations (adapted and modified from Roos 2010).

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desorption, adsorption, and the glass transition may occur during

storage depending on the specific combination of atmospheric

relative humidity and storage temperature Equilibrium of

ambi-ent conditions may only take a few hours or days (Kurtmann and

others 2009b) or as long as to 1 to 2 mo (Fonseca and others

2001) This equilibration period is often not taken into account

in studies with the storage stability and T g At a critical storage

temperature T g, the critical water content and storage relative

hu-midity (or a w) can be determined when information on sorption

isotherm of cells is available (Figure 2 adapted and modified from

Fonseca and others 2001) Information on the sorption isotherm

of dried probiotics is necessary to avoid inactivation due to

mois-ture gain during storage Furthermore, it can be used to

corre-late the storage relative humidity and the final moisture content

of dried cells to avoid unnecessary drying time from drying of

cells far beyond the moisture content corresponding to storage

a w However, in comparison to foods, very little information on

sorption isotherm of probiotics is available Notably, stability of

probiotics is commonly considered with respect to survival The

role of glassy state has never been studied in correlation to probiotic

properties, although the properties are vital for probiotic products

and there is a report about change in the properties during

stor-age The amount of bacteriocin production in freeze-dried vaginal

lactobacillus strains was significantly reduced after storage for 12 mo,

whereas the production of other antimicrobial substances (lactic

acid and hydrogenperoxide) and the auto-aggregation were still

retained (Juarez Tomas and others 2009)

Nevertheless, recent studies on storage of dried probiotics cast

doubt upon the hypothesis that chemical reactions are completely

halted in the glassy state It does not solely determine the storage

stability of dried cells, and inactivation still occurs during storage

at a temperature T – T g = 0 (Higl and others 2007; Kurtmann

and others 2009b) It was suggested that in order to achieve nearly

complete reduction of molecular movements, amorphous

phar-maceutical solids should be stored 50C below T g(Hancock and

others 1995) Similar findings were reported also in a study with

L coryniformis by Schoug and others (2010) and with L rhamnosus

by Miao and others (2008) where viability of cells clearly

de-creased at T – T ghigher than –50C and ca –30C, respectively

Furthermore, the glassy state does not play major protective roleagainst major storage deteriorative reactions such as lipid oxidation(Andersen and others 1999; Kurtmann and others 2009a), becausethe free radical reaction is not diffusion limited In addition, lipidcarbonyls as formed as secondary oxidation products from lipid ox-idation have been suggested to participate in browning reactionsthrough reactions with amino groups in Maillard-like reactions

Browning reaction is related to viability loss in freeze-dried cells(Kurtmann and others 2009c) It was suggested also that the na-ture of the sugar was more important for storage stability than thephysical state of the matrix with the nonreducing sucrose provid-ing better stability than the reducing lactose (Kurtmann and others2009b)

Alternatively, it was also proposed that a biomaterial is most

sta-ble at or below its monolayer moisture content or a w, which varies

in each biomaterial and with environmental conditions (Pitomboand others 1994) For example, the monolayer moisture con-

tent of L bulgaricus (Fonseca and others 2001) and encapsulated

L rhamnosus (Ying and others 2010) was 10% and 3%, respectively.

This concept cannot completely explain the storage stability ofdried cells as well, considering that an increase in temperature sig-nificantly affected the inactivation rate but minimally affected thewater activity Moreover, it provides only information on stronglyassociated and free water but does not indicate when the molecu-lar mobility starts to increase A strong combined effect of wateractivity and temperature was reported and it was suggested that

a w and T g are coupled (Kurtmann and others 2009b) Unlikefreeze-dried proteins, a bacterial cell is not a unique entity butcontains the outside compartment, which is mainly drying ma-trix and the inside compartment, which contains cell componentswith different affinities to water Hence, not all components orfunctions of cells are equally sensitive to moisture or temperature

In other words, there are systems where the inactivation is strongly

Figure 2–Relationships between glass transition temperature, water content, and water activity.

At critical storage temperature a (T g), the

according storage relative humidity (a w) and water content of a sample are b and c (adapted and modified from Fonseca and others 2001).

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Glassy state of dried probiotics

dependent on temperature and others that are strongly depend on

a w(Higl and others 2007)

Conclusion and Outlook

Despite the current opinion that a glassy state is highly

im-portant for the stability of freeze-dried biomaterial and thus has

to be maintained throughout the whole production process and

storage, no study could empirically confirm its decisive effects,

especially in case of probiotics This can be due to the fact that

unlike proteins and foods, dried probiotic cells are largely still

intact and actually separated from the drying matrices Thus,

in case of probiotics, common results relate to the physical state of

the surrounding drying matrices regardless of the actual physical

state of the cytoplasm For a better understanding of the role of the

glassy state on cells, and thus a systematic development of stable

freeze-dried probiotics, further studies are encouraged in order to

elucidate the physical states of cells during production and

stor-age Further studies with practical implication that should also be

addressed are, for example, the role of an annealing step during

freezing, optimal moisture content for stable storage of probiotics,

changes in probiotic properties due to freeze-drying and storage,

and sorption isotherm of dried probiotics

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Nanoemulsions Using Experimental

Mixture Design

Patrick G Maher, Mark A Fenelon, Yankun Zhou, Md Kamrul Haque, and Yrj¨o H Roos

Abstract: The objective of this study was to determine the effect of changing viscosity and glass transition temperature

in the continuous phase of nanoemulsion systems on subsequent stability Formulations comprising ofβ-casein (2.5%,

5%, 7.5%, and 10% w/w), lactose (0% to 20% w/w), and trehalose (0% to 20% w/w) were generated from Design ofExperiments (DOE) software and tested for glass transition temperature and onset of ice-melting temperature in maximallyfreeze-concentrated state (Tg & Tm), and viscosity (μ) Increasing β-casein content resulted in significant (P < 0.0001)increases in viscosity and Tm (P = 0.0003), and significant (P < 0.0001) decreases in Tg  A mixture design was used

to predict the optimum levels of lactose and trehalose required to attain the minimum and maximum Tg  and viscosity

in solution at fixed protein contents These mixtures were used to form the continuous phase ofβ-casein stabilized

nanoemulsions (10% w/w sunflower oil) prepared by microfluidization at 70 MPa Nanoemulsions were analyzed for Tg 

& Tm , as well as viscosity, mean particle size, and stability Increasing levels ofβ-casein (2.5% to 10% w/w) resulted in

a significant (P < 0.0001) increase in viscosity (5 to 156 mPa.s), significant increase in particle size (P = 0.0115) from

186 to 199 nm, and significant decrease (P= 0.0001) in Tg  (−45 to −50C) Increasing the protein content resulted

in a significant (P < 0.0001) increase in nanoemulsion stability A mixture DOE was successfully used to predict glass

transition and rheological properties for development of a continuous phase for use in nanoemulsions

Keywords: glass transition, nanoemulsion, optimization, stability, viscosity

Introduction

Food formulations are widely produced by combining

carbohy-drate, protein, and oil in emulsified systems The characteristics of

individual components can be used to control texture and shelf-life

(Dickinson and Pawlowsky 1997) Structure through glass

forma-tion is provided by carbohydrates Lactose is commonly used for

the continuous matrix-forming material during spray drying It

is a suitable carbohydrate due to its cheap availability, bland

fla-vor, low viscosity in concentrated solutions, and most importantly

its ability to produce a good glass Similarly, trehalose is also a

suitable carbohydrate as it has a wide pH-stability range, and is

nonreducing in the presence of protein during heat treatment

(Higashiyama 2002) Trehalose combined with lactose has been

found to delay lactose crystallization while keeping the glass

tran-sition temperature of powders (Tg) constant (Mazzobre and others

2001), due to modifications to the molecular environment by

ge-ometric, thermodynamic, or kinetic factors Carbohydrates are

often incorporated into dairy protein stabilized nutritional

bev-erages to meet nutritional and structural requirements Typically,

these emulsions are stabilized by amphiphilic moieties, such as

ca-seins The caseins are the most abundant proteins (approximately

Maher and Fenelon are with Teagasc Food Research Centre, Moorepark, Cork,

Ireland Authors Zhou, Haque, and Roos are with School of Food and

Nutritional Sciences, Univ College, Cork, Ireland Direct inquiries to Fenelon

(E-mail: mark.fenelon@teagasc.ie.).

80% w/w) in bovine milk and adsorb strongly at the oil-water terface during homogenization This layer provides stability to theemulsion during processing and storage and prevents coalescence(Dickinson and Stainsby 1982; Vega and Roos 2006) Caseins alsohave low heat sensitivity and better surface-active properties com-pared to whey proteins, which is beneficial for spray drying (Ped-ersen and others 1998; Hogan and others 2001; Dollo and others2003; Sliwinski and others 2003).β-casein is the most hydropho-

in-bic casein, and steric-stabilizing properties of the protein layeraround oil droplets in emulsions are provided by the phosphoser-ine residues ofβ-casein (Dickinson 1997a) β-casein is preferen-

tially adsorbed compared to other caseins due to lower interfacialenergies, and soβ-casein stabilized emulsions are less susceptible

to flocculation (Dickinson and others 1987, 1988; Dickinson andMatsumara 1994) Nanoemulsions are emulsions with a particlesize in the range of 20 to 200 nm that ensures stability as thediffusion rate, due to Brownian motion, is higher than that forsedimentation and creaming (Solans and others 2005)

The glass transition temperature (Tg) is the temperature atwhich, upon heating, an amorphous material changes from a glassy,solid-like state to a rubbery, fluid-like state (Langrish and Wang2006) Glass transition has an effect on many processes and proper-ties encountered in food science In powders, temperatures abovethe glass transition are found to increase the molecular mobilityand free volume, which can result in physico-chemical deteri-oration, such as crystallization of sugars, stickiness, and caking

of powders (White and Cakebread 1966; Slade and Levine 1991).During processing, stickiness may reduce product yields and retardflow of particles leading to operational problems for manufacturing

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equipment and increased down time (Bhandari and Howes 1999).

Also the storage stability and quality changes of food systems are

strongly affected by the glass transition (Schenz 1995)

Crystalliza-tion and caking are time-dependant and are both a funcCrystalliza-tion of

fluctuation in storage temperature and Tg The higher the

tem-perature above the Tg, the more viscosity decreases and molecular

mobility increases leading to crystallization and caking (Bhandari

and Howes 1999; Omar and Roos 2007) These phenomena may

also cause the continuous matrix to become unstable and release

entrapped components, resulting in impaired rehydration

prop-erties (Roos and Karel 1991a) It is therefore important that the

effects of Tgon food materials, such as emulsions in various states

(liquid or dehydrated systems), are taken into account in their

processing and storage

In this study, an experimental mixture design was generated

using Design of Experiments (DOE) software DOE was used

to statistically optimize the formulation of nanoemulsions using

viscosities and glass transition temperatures at fixed protein

con-centrations as response parameters to improve their stability andhence properties as encapsulants Data were analyzed statistically

to show by polynomial equations, adjusted R2and P-values which

variables in the formulation have the most significance on selectedresponses

The objective of this study was to produce nanoemulsions withvarying viscosities and glass transition temperatures at differentprotein levels, and observe the effect on mean particle size andstability through the application of a statistical mixture design

Materials and Methods

D-optimal experimental mixture designThe experimental mixture design was set up using the soft-ware Design Expert R Software version 7.1.3 (Stat-Ease Inc.,Minneapolis, Minn., U.S.A.) A D-optimal design was usedwith the constraints Lactose + Trehalose + β-casein = 20%

w/w with β-casein ≤10% w/w This was used to study the

Table 1– Mixture design formulations of carbohydrate-protein mixtures with experimental results of viscosity (μ at 400 s−1 ) and glass transition (T g  , T m  , T g ) values.

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continuous phase of carbohydrate-protein mixtures prior to

emulsification The model gave 12 different formulations plus

5 replicates leading to a total of 17 experimental

formula-tions (Table 1) These formulaformula-tions contained 20% w/w solids

and were analyzed for viscosity (μ), glass transition

tempera-ture of maximally freeze-concentrated liquid (Tg ), glass

tran-sition temperature of freeze-dried powder (Tg), and onset of

ice melting temperature of maximally freeze-concentrated

liq-uid (Tm ) The software was used to identify the formulations

that both minimized and maximized Tg  and viscosity for the

carbohydrate-protein mixtures at fixed protein concentrations of

2.5%, 5%, 7.5%, and 10% w/w These optimized formulations

(Table 2) were input into the software (Historical Data Initial

Design) with the constraints; Lactose≤ 17.5% w/w, Trehalose

≤ 17.5% w/w, β-casein 2.5% to 10% w/w, where Lactose +

Trehalose+ β-casein = 20% w/w Sunflower oil (10% w/w) was

added to these formulations prior to emulsification

Nanoemul-sions were analyzed for viscosity, Tg , T

m , particle size, and aration rate The data were analyzed graphically and statistically

sep-using the software The statistical significance of the models was

given by the adjusted R2and P-values (Table 3), and the graphical

representations of models (Figure 1 to 8) along with the Scheffe

model polynomial equations for 3 components (Table 4) predict

effects of components in the formulation Models were deemed

significant at P < 0.05.

Carbohydrate-protein mixtures

The materials used in the experiments wereα-lactose

mono-hydrate (Sigma Aldrich, Ireland), trehalose (Cargill, U.K.), and

β-casein (Kerry Group, Ireland) β-casein was dispersed in

dis-tilled water at 45C for 1 h using mechanical agitation, adjusted

for water loss, and stored overnight (12 h) at 4C to ensure protein

hydration Lactose, trehalose, andβ-casein mixtures were prepared

according to Table 1, under mechanical agitation at 55 C for

10 min Formulations were adjusted to pH 7.5 using 1N HCl at

25C

Nanoemulsion preparation

Oil in water nanoemulsions (10% w/w oil) withβ-casein as

emulsifier (2.5% to 10% w/w) were prepared using sunflower

oil (Trilby Trading, Ireland) Coarse emulsions were prepared by

blending 1 L of β-casein solutions with oil at 60 C using a

high shear mixer (Silverson) at approximately 8000 rpm for 2

min Coarse emulsions were microfluidized (model M-110EH,

Microfluidics, Newton, Mass., U.S.A.) using a ceramic interaction

chamber (70 MPa at 60C) Specified quantities of carbohydrates(Table 2) were added to the nanoemulsions in a water bath at 55Cand mixed for 10 min Nanoemulsions were then cooled to 25Cand adjusted to pH 7.5 using 1N HCl The nanoemulsions con-taining lactose, trehalose,β-casein, and sunflower oil according to

the experimental design were heated to 60C and microfluidized

a second time (70 MPa) Approximately 500 mL of sample wascollected and stored at 4C prior to analysis

RheologyRheological analysis of carbohydrate-protein mixtures and na-noemulsions was carried out using an AR G2 rheometer (TAInstruments, Crawley, U.K.), equipped with a 60-mm aluminiumparallel plate (gap 800μm) Samples (approximately 2 mL) were

first presheared at 300 s−1for 1 min and equilibrated for 2 min.Samples were then sheared from 10 to 400 s−1over 3 mins, held

at 400 s−1 for 1 min, and then sheared from 400 to 10 s−1over

3 mins The apparent viscosity, taken at 400 s−1, was used in sequent statistical analysis A shear rate of 400 s−1was chosen tosimulate the conditions of high shear processing All measurementswere carried out at 25C

sub-Differential scanning calorimetry

A differential scanning calorimeter (DSC) equipped with uid N2 cooling (Mettler-Toledo DSC 821e, Schwerzenbach,Switzerland) was used to determine the glass transition temper-atures (onset glass transition temperature of maximally freeze-concentrated solids, Tg , for liquids and onset glass transitiontemeparture, Tg for anhydrous samples) and onset temperatures

liq-of ice melting in maximally freeze-concentrated solids (Tm ) incarbohydrate-protein mixtures and nanoemulsions Samples wereprepared in preweighed aluminium pans (40μL; Mettler Toledo-

27331) and scanned in hermetically sealed pans An empty panwas used as a reference The DSC was calibrated for temperatureusing n-hexane (melting point, 95.0C), mercury (melting point,

−38.8 C), water (melting point, 0.0 C), gallium (melting

point, 29.8C), and indium (melting point, 156.6C), and forheat flow using n-hexane (Hm, 151.8 J/g), mercury (Hm,11.4 J/g), water (Hm, 334.5 J/g), gallium (Hm, 80.0 J/g),and indium (Hm, 28.45 J/g) Liquid samples were hermeticallysealed in aluminium pans (40μL; Mettler Toledo) with an empty

pan as reference and scanned from−100C to 25C to

deter-mine Tg and Tm for nonannealed samples Samples were thenannealed for 15 min at approximately 1C below the initial onset

of Tm(measured during the 1st temperature cycle), followed by a

Table 2–Optimized formulations for minimum and maximum viscosity (μ at 400 s−1 ) and glass transition temperature (T g  ) for sions at fixedβ-casein contents (2.5%, 5%, 7.5%, 10% w/w).

nanoemul-Lactose Trehalose β-casein Mean particle μEmul T g T m Separation rate Stokes’ creaming

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m  Anhydrous samples were prepared by freeze drying

the carbohydrate-protein mixtures at their various concentration

levels They were 1st heated over the glass transition

tempera-ture region (60 to 140C), then cooled to below glass transition

temperature, and a 2nd heating scan was run over the glass

transi-tion region and the Tgwas measured Heating and cooling rates

for both liquid and anhydrous samples were 5 C/min and 10

C/min, respectively T

g, Tg , and T

m  were determined usingSTARethermal analysis software, version 8.10 (Mettler Toledo)

Measurements were carried out in triplicate

Particle size analysis

Particle size of the nanoemulsions was measured using a

Zetasizer Nano system (Malvern Instruments, Inc., Worcester,

U.K.) Measurements were carried out at 22 C, at a

scatter-ing angle of 173 Samples were diluted using distilled water by a

factor of 20 prior to analysis to avoid the effects of multiple

scat-tering The mean average (z-average) droplet size was measured

using an intensity distribution

Stability analysis

A Lumifuge 116 stability analyzer (L.U.M GmbH, Berlin,

Germany) was used to measure the separation rate of

nanoemul-sions at 25C The Lumifuge is an analytical centrifuge that

con-tinually measures the light transmitted through a sample over the

Table 3–Statistical significance of models, both transformed and

un-transformed, for carbohydrate-protein mixtures and nanoemulsions.

Model significance Carbohydrate

a The natural log, (ln), of the viscosity results for the carbohydrate-protein mixtures was

modeled and the given R2 values reflect this transformed result.

b The inverse square root of the nanoemulsion viscosity results was modeled and the given

R2 values reflect this transformed result.

c Viscosity measurements are quoted at 400 s −1.

total length of the measurement cell The samples (0.4 mL aliquots)were placed in polycarbonate sample cells and centrifuged (1140

× g) for approximately 7.2 h, simulating 1 y of separation

un-der normal gravity Separation rates were determined using thesoftware package SepView 4.1 (L.U.M GmbH), which calculatedthe velocity of the separation of the individual particles from themeasurement results (μm/day)

Results and Discussion

Viscosity of carbohydrate-protein mixturesThe effect of increasingβ-casein content (0% to 10% w/w)

on viscosity is represented graphically in Figure 1 Viscosity creased exponentially with increasing protein content from 2 to

in-78 mPa.s, possibly as a result of increased interactions betweenhydrated protein molecules (Boye and others 1997) and the ability

of protein molecules to absorb water and swell (Damodaran 1997).Mora-Gutierrez and Farrell Jr (2000) suggested that sugarmolecules (lactose and sucrose) do not bind to proteins (casein),

or affect viscosity in protein-sugar systems However,

trehalose-β-casein mixtures had higher viscosity than lactose-trehalose-β-casein

mix-tures at equivalent carbohydrate contents (Table 1)

The data for viscosity analysis were fitted with a special cubicmodel, which was transformed using a natural log power law rec-ommended by the Box-Cox method This minimized the residualsum of squares in the model, thus improving the statistical analy-

sis The model was significant (P < 0.0001) with a high adjusted

R2(Table 3) The coefficients for this coded Scheffe polynomialmodel are shown in Table 4 and together with the ternary diagramand three-dimensional (3D) surface diagram in Figure 1 show that

β-casein (component C) had the greatest effect on viscosity Low

viscosity systems are the desired outcome The results show thatlow viscosity systems can be produced with lower quantities ofprotein (≤ 5% w/w) The negative coefficients (Table 4) and thedownward curves (Figure 1) for the nonlinear blending terms

AC and BC show that there is synergism between lactose with

β-casein, and between trehalose with β-casein, meaning that these

binary mixtures can result in low viscosity The antagonism ofadding a third component to the mixture causes an increase inviscosity (positive ABC)

Glass transition of carbohydrate-protein mixturesThe glass transition temperatures (Tg ) of the maximally freeze-concentrated carbohydrate-protein mixtures decreased with in-creasing protein content (Table 1; Figure 2) It is likely that

Table 4– Coefficients for each term in the coded polynomial equation, both transformed and untransformed, for carbohydrate-protein mixtures and nanoemulsions.

Coded polynomial equation coefficients for Scheffe model Carbohydrate

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increased viscosity retarded ice formation, thus decreasing the

so-lute concentration at maximum freeze concentration, Cg  This

diluted the unfrozen matrix, and therefore the Tg decreased due

to the higher plasticizing effect of unfrozen water (Roos and Karel

1991b)

A special cubic model was used to fit the data for Tg ,

giv-ing significance at P < 0.0001 with a high adjusted R2 value

(Table 3).β-casein had the greatest effect on Tg , as demonstrated

by the negative 2nd-order nonlinear blending terms involving

β-casein (AC and BC) compared to the positive coefficient for model

term AB (Table 4; Figure 2) A high Tg is the desired outcome

for solutions Therefore, there is antagonism between lactose with

β-casein, and between trehalose with β-casein Varying the ratio

of lactose to trehalose had little effect on Tg at fixed protein levels.

The synergism of adding a 3rd component to the mixture causes

an increase in Tg , as indicated by the positive coefficient for the

three component nonlinear blending term from Table 4 (ABC) It

is suggested that increased viscosity is the primary reason for Tg 

decrease with increasing protein content

The onset temperature of ice melting in the maximally

freeze-concentrated state, Tm , is an important property of a material

as it is the “mobility” point (Reid and others 1994) or point

at which the structure begins to collapse under its own weight

during freeze drying (Kaushik and Roos 2007) Tm  increased

with increasing protein content (Table 1; Figure 3) As ice forms,

freeze-concentration of solids occurs simultaneously, decreaseing

the freezing/melting temperature of the unfrozen water (Roos

2007) Increasingβ-casein contents retarded ice formation with

a resultant lower Tg and higher T

m (ice formation ceased at ahigher temperature which corresponded to the higher Tm ) Roos

and Karel (1991b) found that in sucrose solutions ice formation

ceased at a viscosity of 107Pa s Although viscosities of the

freeze-concentrated carbohydrate-protein mixtures were not measured,

it is likely that the viscosities increased with the decreasing

temper-ature and increasing solids content of the unfrozen phase during

freeze concentration

The data for Tm  analysis were fitted with a quadratic model

and had a high adjusted R2 with significance at P = 0.0003

(Table 3) β-casein had a greater effect on Tm  than the vidual sugars (Table 1; Figure 3) Similar AC and BC values and

indi-a smindi-all coefficient for model term AB show thindi-at indi-at fixed proteinlevels, the ratio of lactose to treahlose is irrelevant It is suggestedthat increased viscosity is the biggest factor in increasing Tm ,therefore, it is beneficial to have highly viscous systems to produce

a high Tm .For freeze-dried powders, Tgincreased with increasing proteincontent (Table 1; Figure 4) The lowest protein content (2.5%w/w) system in the present study had a Tg of approximately

104C, whereas the highest protein content (10% w/w) systemhad a Tg of 124C Biliaderis and others (2002) reported thatthe addition of a high molecular weight carbohydrate (pullalan) tolactose increased Tg Similarly, Shamblin and others (1996) foundthat the Tg of sucrose solutions was higher in the presence ofpolymeric substances, such as starch and polyvinylpyrrolidone

A quadratic model was fitted to the data for Tgwith significance

at P < 0.0001 with a high adjusted R2(Table 3) Component C(β-casein) again had the most significant effect on Tg (Table 4;Figure 4) High Tgvalues are favorable in dairy powders, so highprotein systems give a beneficial outcome in this respect.The presence of protein in either liquid or dehydrated systems,affects the glass transition temperature of that system Typically, ahigh Tg in a liquid system should correspond to a high T

gpostdehydration Similarly, a low Tg should correspond to a low T

gpost dehydration In the current work, increasing protein contentincreased the Tg for dehydrated systems (Figure 4) while it de-creased Tg for liquid systems (Figure 2) As previously discussed,this may be due to increased solution viscosity at higher proteinconcentrations, which makes ice crystal formation more difficult,thus more unfrozen water remains in the continuous phase lower-ing Tg  Therefore, the glass transition temperatures in both liquidand dehydrated forms are strongly influenced by protein content

Particle size of nanoemulsionsFor the nanoemulsions, mean particle size increased significantlywith increasing protein content (Table 2; Figure 5) Particle size

Figure 2 – Contour and response surface plots of onset glass transition temperature of maximally freeze-concentrated solids (T g) in protein mixtures comprising of lactose, trehalose, andβ-casein (0% to 20% w/w).

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increased from approximately 187 to 199 nm for increasing protein

contents up to 7.5% w/w β-casein, however mean particle size

decreased to 193 nm for samples containing 10% w/wβ-casein.

The general trend toward increased mean particle size may be due

to a layering affect of the protein around the small oil droplets

according to self-consistent field (SCF) theory This occurs when

the bulk protein concentration goes above a certain threshold value

(depending on ionic strength), causing multilayer condensation of

self-associating protein onto the oil droplet surface (Dickinson

1997a) In contrast with the current study, Qian and McClements

(2011) found that mean particle size decreased with increasing

protein content for sodium caseinate stabilized nanoemulsions,

however, they did obtain a similar narrow size distribution

The data for particle size were fitted with a quadratic model

and was significant (P < 0.0115) with a high adjusted R2

(Table 3) β-casein is the only component in the mixture that

affects particle size Lactose and trehalose are hydrophilic and main in the continuous phase, therefore having no direct effect

re-on particle size This is seen in Table 4 with the low negativecoefficient value for model term AB

Viscosities of nanoemulsionsThe viscosity of the nanoemulsions increased with increasingprotein content (Table 2, Figure 6) This was most likely due

to increased protein–protein interaction in the continuous phase

as the protein content increases The addition of sunflower oil

to the system increased the solids content by 10% (that is, 30%solids in total) and so the nanoemulsions are more viscous thanthe carbohydrate-protein mixtures

Figure 3–Contour and response surface plots of onset temperature of ice melting (T m) in carbohydrate-protein mixtures comprising of lactose, trehalose, andβ-casein (0% to 20% w/w).

Figure 4–Contour and response surface plots of glass transition temperature of freeze-dried powder (T g ) in carbohydrate-protein mixtures comprising

of lactose, trehalose, andβ-casein (0% to 20% w/w).

Trang 15

A quadratic model was fitted to the viscosity data, which was

transformed using an inverse square-root power law recommended

by the Box-Cox method The model was significant (P < 0.0001)

with a high adjusted R2 (Table 3) The results again show that

low viscosity nanoemulsions (< 15 mPa.s) can be produced at

protein contents of≤ 5% w/w The negative coefficients (Table 4)

and the downward curves (Figure 6) for the nonlinear blending

terms AC and BC show that there is synergism between lactose

with β-casein, and between trehalose with β-casein, meaning

that these emulsions can keep a low viscosity The viscosities of

the nanoemulsions in Table 2 show that varying the level of lactose

to trehalose, at fixed protein levels, gave similar viscosities

Glass transitions of nanoemulsions

The Tg of the nanoemulsions decreased as protein content was

increased (Figure 7), in agreement with results for

carbohydrate-protein mixtures (Figure 2) The experimental Tg values for thenanoemulsions are similar to the Tg values predicted for the mix-tures by the optimization function in the DOE software Thisshows that sunflower oil did not affect Tg  most likely becausethe oil was in the dispersed phase, while the continuous phase isprimarily responsible for changes in Tg .

The data for Tg were fitted with a quadratic model, and it was

significant (P= 0.0001) with a high adjusted R2(Table 3) Thelarge negative coefficients for the 2nd-order nonlinear blendingterms (Table 4) involvingβ-casein (AC and BC) compared to the

smaller AB value show that β-casein had the greatest effect on

Tg  It was found that there is antagonism between lactose with

β-casein, and between trehalose with β-casein, as previously seen

for the carbohydrate-protein mixtures Therefore, low quantities

ofβ-casein combined with lactose or trehalose give the largest Tg .The ratio of lactose to trehalose in the emulsion, at fixed protein

Figure 5–Contour and response surface plots of mean particle size in nanoemulsions comprising of lactose, trehalose, andβ-casein contents.

Figure 6–Contour and response surface plots of viscosity (at 400 s−1) in nanoemulsions comprising of lactose, trehalose, andβ-casein contents.

Trang 16

contents, is irrelevant as indicated by the relatively low coefficient

AB in Table 4 The decrease in Tg with increasing protein content

can be explained by a concomitant increase in viscosity

The Tm for nanoemulsions differed from those found for the

carbohydrate-protein mixtures In this case, the Tm  decreased

with increasing protein content and the Tm values were lower in

each case for the nanoemulsions (Table 2), compared to that of

the carbohydrate-protein mixtures (Table 1) The overall model

generated was not significant at P = 0.0631 (Table 3), which

meant that the overall mean was a better predictor of the response

than the current model

Nanoemulsion stability

The nanoemulsion stability was measured by analyzing the

flota-tion/creaming rates of particles using an analytical centrifuge The

highest protein content nanoemulsions (7.5% and 10% w/w

pro-tein) were the most stable with separation rates of 7 and 4μm/d,

respectively, compared to separation rates of 41 and 24μm/day

for nanoemulsions with 2.5% and 5% w/w protein contents,

re-spectively (Table 2; Figure 8) Nanoemulsions are reported to

be more stable to creaming on storage compared to

microemul-sions due to the effects of Brownian motion being stronger than

gravitational forces They are also more stable to flocculation and

coalescence due to the lowering of the interfacial tension with

de-creasing particle size that decreases the stress required to break up

the droplets Typically, casein-coated emulsion droplets are prone

to depletion flocculation at protein concentrations higher than 2%

w/w (Dickinson and Golding 1997) This could be due to the

effect of unadsorbed casein in the continuous phase that passes

between oil droplets causing an osmotic pressure gradient, that

entropically force out the aggregated casein, causing the droplets

to flocculate (Dickinson 1997b, 1999) Increasing protein content

increases the occurrence of depletion flocculation In some cases,

it has been found that stability decreases with increasing sodium

caseinate content up to a certain concentration (6% w/w) Above

this concentration a more rigid structure is formed, preventing

rapid creaming (Dickinson and others 1997)

Experimental separation rates were compared to those lated using Stokes’ law equation (see Table 2):

calcu-v s = (ρf − ρ p)

where vs is the separation velocity of the particles, (ρf − ρp) isthe difference between the densities of the fluid in the continuousphase (1060 kg.m−3) and the particles of oil (917 kg.m−3), g is

gravitational acceleration (9.81 m.s−2), dpis the mean particle ameter (m), andμ is the viscosity of the nanoemulsion (kg/(m.s)).

di-The units are converted toμm/day and compared with the

exper-imental separation rates calculated from the Lumifuge in Table 2 Itwas also observed that as particle sizes of nanoemulsions were verysimilar overall that viscosity was the primary factor in determiningthe separation rate In general, the results compared well, howeverStokes’ law is applicable for ideal systems and this system is notideal due to hindrance caused by concentration effects (Robins2000)

A cubic model was fitted to the data for nanoemulsion stability

with significance at P < 0.0001 with a high adjusted R2 value(Table 3).β-casein had the most significant effect on nanoemulsion

separation rate due to increased viscosity at high protein levels Thenegative coefficients (Table 4) and the downward curves (Figure 8)for the nonlinear blending terms AC and BC show that there issynergism between lactose withβ-casein, and between trehalose

with β-casein, meaning that these mixtures can maintain low

separation rate The quantity of lactose or trehalose has no effect

on stability as indicated by the small coefficient for the modelterm AB

Overall, the desired result from an emulsion system is ideally toproduce a low viscosity, high Tg , that when dried corresponds

to a high Tg, low mean particle size and low separation rate

A fine balance can be achieved, whereby a low viscosity, highlystable emulsion system can be produced that is not susceptible

to physico-chemical deteriorative changes that are caused by lowglass transition temperature This study has demonstrated how tostatistically optimizeβ-casein stabilized nanoemulsion systems.

Figure 7–Contour and response surface plots of glass transition temperature of maximally freeze-concentrated solids in nanoemulsions (T g) comprising

of lactose, trehalose, andβ-casein.

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A statistical mixture design was successfully used for the

for-mulation of nanoemulsions based on optimization of

continu-ous phase parameters of viscosity and glass transition The study

showed that increasing β-casein content in mixtures containing

lactose and trehalose, significantly (P < 0.0001) increased

viscos-ity and decreased glass transition Tg  A similar trend was observed

inβ-casein stabilized nanoemulsions containing lactose and

tre-halose This indicates that the physical properties of the continuous

phase are a primary factor influencing the stability and

function-ality of subsequent emulsions Nanoemulsion mean particle size

(P < 0.0115) and stability (P < 0.0001) were significantly

in-creased with increasingβ-casein content It was postulated that

the increased stability was due to the effect of increased viscosity

that reduced the separation rate of the dispersed phase according to

Stokes’ law Modulation of glass transition temperatures through

selection of ingredients, and their concentrations, may be

benefi-cial in powdered products to combat the phenomena of stickiness

and crystallization during storage

Statistical experimental mixture design can be a useful tool in

the formulation of nanoemulsions It reduces the workload by

giving a set number of experiments, and determines and analyzes

the impact of each component in the mixture

Acknowledgments

This research has been funded by the Irish Dept of Agriculture,

Fisheries & Food under the Food Institutional Research Measure

(FIRM)

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Nutritional Characteristics of Seed

from Southern Spain

Elena Pastor-Cavada, Rocio Juan, Julio E Pastor, Manuel Alaiz, and Javier Vioque

Abstract: The study of local plants could provide useful data for the possible development of future crops with good

nutritional and functional properties The nutritional characteristics of the seed proteins of 28 Vicia species (31 taxa) (Fabaceae) from Spain were studied Protein contents in studied Vicia ranged from 20.1% in V articulata to 32% in

V pyrenaica V altissima, which is only deficient in Trp, showed the most balanced amino acid composition, while the remaining taxa were limiting in Met, Cys, and Trp In vitro protein digestibility (IVPD) ranged from 78% in V incana to 86.3% in V hirsuta In addition to the amino acid composition and IVPD, other nutritional parameters, such as amino acid

score, biological value, protein efficiency ratio, or protein digestibility corrected amino acid score, were studied Results

confirm the interest of studying wild populations of cultivated and non cultivated Vicia species as potentially interesting

sources of seeds with good nutritional characteristics

Keywords: amino acids, nutritional quality, seed proteins, Vicia

Introduction

Legume seeds may represent an important source of protein,

di-etary fibre, carbohydrates, several vitamins, and minerals (Granito

and others 2007; Mart´ın-Cabrejas and others 2008) Legumes can

be used for feeding livestock, for human food, or to increase the

ni-trogen levels in soil In several regions of the world, legumes play an

important role in human and animal nutrition as they are a cheap

source of protein and other nutrients (Cerletti and others 1978)

In recent years, several researchers, such as Rochfort and Panozzo

(2007), have shown that the consumption of proteins, certain

lipids, polyphenols, or bioactive peptides contained in legumes has

a beneficial effect on health According to Duranti (2006), legumes

may prevent diseases such as diabetes mellitus, colon cancer, and

coronary heart diseases Due to the presence of many beneficial

components in pulses, these positive effects can be related to more

than one compound For example, the cardio-protective effect of

pulses may be due to the synergistic effect of different compounds,

such as bioactive peptides or free fatty acids Although

consump-tion of legumes had been decreasing in many Western countries,

their high nutritional value has led to a recent increase in their

use in the human diet In addition, since the “green revolution,” a

large amount of the world’s phytodiversity has been lost because

lo-cal crops have been substituted by other genetilo-cally uniform crops,

which have higher yields However, the diversification of cultivars

is necessary to adapt cultivars to soil and water conditions, or to

limit phytosanitary risks Hence, knowledge of local plants could

provide useful data for the possible development of future crops

MS 20101443 Submitted 12/22/2010, Accepted 6/29/2011 Authors

Pastor-Cavada, Alaiz, and Vioque are with Inst de la Grasa (C.S.I.C.), Avda

Padre Garc´ıa Tejero 4, 41012-Sevilla, Spain Authors Juan and Pastor

are with Dept de Biolog´ıa Vegetal y Ecolog´ıa, Univ de Sevilla,

41012-Sevilla, Spain Direct inquiries to author Pastor-Cavada (E-mail: epastor@cica.es;

epastor@ig.csic.es).

The Vicia genus is a legume with more than 140 species Some Vicia species have been used as livestock feed or as a green manure

crop, and others have been used for local consumption For

example, the seeds of V articulata, V ervilia, V hirsuta, V monantha,

V narbonensis, or V sativa have been consumed in the past In other cases, the green parts are consumed, such as the leaves of V hirsuta,

V narbonensis, or V sativa In the latter species the leaves have been employed as a tea substitute Vicia species have also been inves-

tigated as sources of antioxidant compounds such as polyphenols(Pastor-Cavada and others 2010) The most commonly consumed

species is V faba, which is broadly cultivated in the Mediterranean

Region for human nutrition and livestock feed and studies on the

use of V faba for animal fodder have been carried out (Palander and others 2006) The protein fraction of V faba has also been

extensively characterized, including the amino acid composition(Lattanzio and others 1983), functional properties (Cepeda andothers 1998), the production of protein isolates (Macarulla andothers 2001), and protein hydrolysates (Chakraborty and others1979)

However, apart from V faba, there are very few studies on the

nutritional quality of seed proteins in wild populations of either

cultivated or noncultivated Vicia species.

In this study, the amino acid composition and nutritional

qual-ity of seed proteins were studied in 28 Vicia species (31 taxa)

distributed throughout Southern Spain Results provide useful formation concerning which of the species that are or were locallycultivated possess better nutritional properties in their seed pro-teins, and which wild taxa could be of interest from a nutritionalpoint of view

in-Material and Methods

MaterialsTrypsin, chymotrypsin and peptidase were from Sigma (TresCantos, Madrid, Spain) Diethyl ethoxymethylenemanolate waspurchased from Fluka (Buchs, Suiza) All other chemicals were of

Trang 20

analytical grade Vicia seed samples were taken from wild

popu-lations except V faba, which was purchased from a local market.

Voucher specimens of studied populations are deposited in the

Herbarium of the Dept of Plant Biology and Ecology of the

Univ of Seville

Flour preparation

Select grains were milled using a grinder to obtain a uniform

flour

Protein estimation method

Total nitrogen was determined by the micro Kjeldahl method

according to AOAC (1999) 960.52 approved method Crude

pro-tein content was estimated using a conversion factor of 6.25 for

legumes

Amino acid analysis

Samples (10 mg) were hydrolyzed with 4 mL of 6 N HCl The

solutions were sealed in tubes under nitrogen and incubated in an

oven at 110 C for 24 h Amino acids were determined after

derivatization with diethyl ethoxymethylenemalonate by

high-performance liquid chromatography (HPLC), according to the

method of Alaiz and others (1992), using D,L-α−aminobutyric

acid as an internal standard The HPLC system consisted of a

Model 600E multi-system with a 484 UV–vis detector (Waters,

Milford, Mass., U.S.A.; EEUU) equipped with a 300× 3.9 mm

i.d reversed-phase column (Novapack C18, 4μm; Waters) A

bi-nary gradient was used for elution with a flow of 0.9 mL/min

The solvents used were (A) sodium acetate (25 mM) containing

sodium azide (0.02%, w/v) pH 6 and (B) acetonitrile Elution was

as follows: time 0 to 3 min, linear gradient from A/B (91 : 9)

to A/B (86 : 14); 3 to 13 min, elution with A/B (86 : 14); 13 to

30 min, linear gradient from A/B (86 : 14) to A/B (69 : 31); 30 to

35 min, elution with A/B (69 : 31) The column was maintained

at 18C Tryptophan was analyzed by HPLC after basic hydrolysis

according to Yust and others (2004)

In vitro protein digestibility

In vitro protein digestibility (IVPD) was determined according

to the method of Hsu and others (1977) Samples containing

62.5 mg of protein were suspended in 10 mL of water and

the pH was adjusted to 8 An enzymatic solution containing

1.6 mg trypsin (17.7 BAEE U mg– ), 3.1 mg α-chymotrypsin

(43 U mg– ) and 1.3 mg peptidase (50 U g– ) per milliliter was

added to the protein suspension in a 1 : 10, v/v, ratio The pH of

the mixture was measured after 10 min, and the in vitro

digestibil-ity was calculated as a percentage of digestible protein using the

equation: % digestible protein= 210.464 – 18.103 × pH

Determination of nutritional parameters

The amino acid composition of studied Vicia was used for the

determination of several nutritional parameters of Vicia seed

pro-teins:

(1) Amino acid score (chemical score) was calculated as: %

sample essential amino acids contents /% recommended

essen-tial amino acids (FAO/WHO/UNU 1985)

(2) Protein efficiency ratio (PER) values were calculated from

the amino acid composition of Vicia seeds based on the following

3 equations (Alsmeyer and others 1974):

PER1= − 0.684 + 0.456 × Leu − 0.047 × Pro

PER2= − 0.468 + 0.454 × Leu − 0.105 × Tyr

PER3= − 1.816 + 0.435 × Met + 0.78 × Leu

± 211 × Hys − 0.944 × Tyr

(3) Protein digestibility corrected amino acid score (PDCAAS)(FAO/WHO 1989) was calculated as:

PDCAAS= Lowest uncorrected amino acid score × IVPD.

Uncorrected amino acid score= milligram of essential aminoacid in 1 g of test protein per milligram of essential amino acid in

1 g of reference protein (FAO/WHO/UNU 1985)

(4) Predicted biological value (BV) was calculated according toMorup and Olesen (1976) using the following equation:

BV= 102.15× Lys0.41× (Phe + Tyr)0.60× (Met + Cys)0.77

× Thr2.4× Trp0.21

where each amino acid symbol represents:

% amino acid/% amino acid FAO pattern(FAO/WHO/UNU

1985),

if % amino acid= % amino acid FAO pattern or

% amino acid FAO pattern (FAO/WHO/UNU 1985)/% aminoacid,

if % amino acid= % amino acid FAO pattern.

Cluster analysisResults are expressed as the mean values± SD of several sam-ples except for species with only 1 population Cluster analysis ofdifferent taxa was performed using PRIMER-pc program, em-ploying the Bray–Curtis index of dissimilarity (Bray and Curtis1957) The dissimilarity index was transformed to the index ofsimilarity (1 – dissimilarity index)× 100

Results and Discussion

Vicia seed protein contents ranged from 20.1% in V articulata to 32% in V pyrenaica (Table 1) These percentages observed in wild populations are similar to those reported for Vicia seeds belonging

to cultivated species such as V sativa In a screening of 840 V faba

lines, protein contents ranged from 18% to 31% with an averagecontent of 24% (Elsherbeeny and Robertson 1992) In addition,

the protein contents of several of the studied Vicia were also higher

than those observed in other cultivated legumes such as chickpeawith 24.7% seed protein ( S´anchez-Vioque and others 1999)

Amino acid composition of Vicia is shown in Table 1 Vicia species show an amino acid pattern characteristic of legumes

(Carbonaro and others 1997) According to FAO tions (FAO/WHO/UNU 1985), all taxa examined are deficient

recommenda-in sulfur amrecommenda-ino acids (Met and Cys) and Trp, except V altissima,

which was only deficient in Trp

In studied Vicia taxa, the most abundant essential amino

acids in decreasing order were Leu, Lys, Phe, Thr, and

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Val Leu values in all taxa are above FAO recommendations

(FAO/WHO/UNU 1985), with the highest contents observed in

V pubescens, which were significantly different (P < 0.05) from

those observed in V pseudocracca (Table 1) Lys, was not

limit-ing in any studied Vicia, with the highest percentages observed

in V ervilia, which were significantly different (P < 0.001) from

those observed in V eriocarpa and V vicioides Contents in aromatic

amino acids, Phe and Tyr, are also above FAO recommendations

(FAO/WHO/UNU 1985) These contents were similar in all

studied taxa, and only in V hybrida Phe percentages were

signifi-cantly different (P < 0.05) from those observed in V angustifolia,

V sativa subsp Sativa, and V tenuifolia His, Ile, and Val contents

are similar in all studied species with values in all cases above FAO

recommendations (FAO/WHO/UNU 1985)

Among the studied species, V altissima appears as the one with

the most balanced amino acid composition, because it was only

deficient in Trp Among the remaining taxa, V benghalensis and

V glauca subsp giennensis showed the best sulfur amino acids

con-tents (Table 1)

The importance of protein composition in the diet has been

well known for many years The nutritional quality of proteins

depends mainly on the amino acid composition To make use of

these amino acids, proteins must be digested to release them The

protein quality, also known as the nutritional or nutritive value of a

food, depends on its amino acid content and on the physiological

utilization of these amino acids after digestion and absorption

Many different factors may impair protein digestibility Hence, in

addition to amino acid composition, protein digestibility is another

protein characteristic which determines the protein quality

In vitro methods of protein evaluation are useful for determining

the nutritional value of new protein foods because they are faster

than in vivo methods (Monsoor and Yusuf 2002) Hsu and others

(1977) used a method that obtains in vitro digestibility value which

has high correlation with in vivo digestibility observed in rats.

IVPD in studied Vicia species ranged from 78% in V incana to

86.3% in V hirsuta (Table 2) Among the studied taxa, 14 of them

showed an IVPD higher (Table 2) than V faba (83.2%), which is

the most cultivated species Furthermore, most possessed an IVPD

higher than those observed in other legumes such as chickpea

(76.2%) (S´anchez-Vioque and others 1999), or other crops, such

as Amaranthus cruentus (77%) (Betschart 1982) or rapeseed (72.8%)

(Larbier and others 1991)

The highest Biological Value was observed in V benghalensis with

values of 67, whereas the lowest was observed in V hybrida with

18.7 (Table 2) The best biological values observed in this study

were similar to those reported in cereals such as wheat (61.6)

or triticale (65.3) (Friedman 1996), although lower than those

described for lactoalbumin (97%)

The PER is a good method for evaluating protein quality PER

values were calculated according to the formulae proposed by

Alsmeyer and others (1974), which have been shown to bear a

good relationship with real PER values The best PER values

were observed in V pubescens with PER1, PER2, and PER3 of

3.27, 3.29, and 3.77, respectively The lowest values were

calcu-lated for V tenuifolia with PER1 of 2.51 and PER2 of 2.58, and

V eriocarpa with PER3of 2.20 Similar values to those reported

here for Vicia have been described for other legumes (Alsmeyer and

others 1974) In this way, Sujak and others (2006) used PER2to

evaluate protein quality of Lupinus angustifolius (2.36) and Lupinus

albus (2.87).

The use of amino acid scores has been proposed as a more

ac-curate alternative to PER parameters (Sarwar and others 1984)

The chemical score is a simplified model for predicting dietaryprotein quality, but it does not take into account amino acid di-gestibility or availability (Moughan 2005) The amino acid score

was the highest in V hybrida with an average value of 129.5 (Table 2) The lowest value was observed in V benghalensis and

V eriocarpa with average values of 114.2 In a similar way, the % essential amino acids/total amino acids ratio was the highest in V hybrida with average values of 43.9, while the lowest was observed

in V benghalensis with average values of 38.8.

The PDCAAS is nowadays the most recommended theoreticalparameter for evaluating the nutritional quality of food proteins

It is based on FAO recommendations of amino acids requirements(FAO/WHO/UNU 1985) and IVPD It is superior to other meth-ods for evaluating the protein quality of food for humans because

it determines the quality of a protein based on the amino acidrequirements of a 2- to 5-year-old child adjusted for digestibility.The highest PDCAAS value for a given protein is 1.0, this proteinwill provide 100% of the indispensable amino acids recommended

by FAO/WHO (1989), however values≥ 0.5 are considered quite

good PDCAAS values in Vicia ranged from 0.32 in V faba to 0.55

in V lutea subsp vestita (Table 2) Most studied taxa have an

essen-tial amino acid composition similar or better in some indispensable

amino acid, like sulfur amino acids, than V faba Eleven of the

stud-ied taxa have a high nutritional quality proteins (PDCAAS≥ 0.5)(Table 2), showing similar PDCCAS values to those observed inother legumes, such as lentil (0.52) although lower than pea (0.69)(Henley and Kluster 1994)

Among mentioned taxa, V cordata, V lutea subsp vestita,

V monantha subsp calcarata, and V peregrina should be taken into

account because they have a good production of wild seeds withgood average size They have a balanced amino acid compositionand a high IVPD too Finally, all of them have a PDCAAS≥ 0.53,which is considered a good value and higher than value from

V faba (0.32), which is the most used as commercial legume.

The analysis of similarity of studied Vicia, based on seed protein

essential amino acid composition, shows that studied taxa have an

affinity higher than 93% (Figure 1) V vicioides (group A) clearly differs from all other Vicia taxa (group B), basically because of its high Thr contents Although V monardi also has also high percentages of Thr, it differs from V vicioides in its lower content

of Val and Ile (Table 1) Within group B another group (C) is

distinguished with a 94.6% affinity Group C includes V faba,

V pubescens, V hirsuta, V articulata, V ervilia, and V parviflora, which

are all annual species These species are characterized by higheramounts of Leu and lower amounts of Val in the seed proteins.Among the remaining taxa (group D), 3 groups (E, F, and G) weredistinguished Group E is formed by perennial species, except

V monardi, which is annual They tend to have higher contents

of Thr, ranging from 5.3 in V pyrenaica to 6.1 in V monardi.

Species in groups F and G are clearly distinguished due to thefact that those included in group F show higher contents of Phe,Ile, and Lys compared to those in group G In general, in bothgroups annual species predominate, although some species are

perennial such as V altissima in group F or V onobrychioides in group

G Group G is subdivided into 2 groups with all taxa belonging

to V lutea clustered in subgroup G2.

Species that are or have been used in crops in the past arelocated in groups C and F Although in other plant genera, such

as Teucrium, the amino acid composition has been useful from a

taxonomic point of view (Juan and others 2004), this was not so

in the case of Vicia Thus, clusters in Figure 1 do not correlate with recognized sections in the Vicia genus.

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Nutritional characterization of studied Vicia seed proteins shows

that these pulses have seed proteins of a high nutritional quality,

similar to those observed in other legumes and crops This

infor-mation may be useful for the revalorization of the Vicia species,

which were more broadly cultivated in the past It may also even

help in the domestication of new species or the use of wild

pop-ulations in breeding programmes, favoring the bioconservation of

Vicia.

References

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(Vicia faba) on the cholesterol metabolism of hypercholesterolaemic rats Brit J Nutr 85:607–14.

Mart´ın-Cabrejas M, D´ıaz MF, Aguilera Y, Ben´ıtez V, Moll´a E, Esteban RM 2008 Influence

of germination on the soluble carbohydrates and dietary fibre in non-conventional legumes Food Chem 107:1045–52.

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chickpea (Cicer arietinum L.): chemical composition, functional properties and protein

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Trang 26

Discrimination of Chinese Vinegars Based

on Headspace Solid-Phase Microextraction-Gas

Chromatography Mass Spectrometry of Volatile

Compounds and Multivariate Analysis

Zuobing Xiao, Shuiping Dai, Yunwei Niu, Haiyan Yu, Jiancai Zhu, Huaixiang Tian, and Yongbo Gu

Abstract: Headspace solid-phase microextraction (HS-SPME) coupled with gas chromatography mass spectrometry

(GC-MS) was applied for the determination of the characteristic volatile profiles of Chinese vinegars Multivariate

statistical techniques, such as principal component analysis (PCA) and cluster analysis (CA), were used to characterize

the different Chinese vinegars by types, fermentation method, and production area A total of 56 volatile compounds

were identified, including 15 esters, 10 aldehydes, 5 acids, 12 alcohols, 5 ketones, 4 volatile phenols, 2 pyrazines,

and 3 miscellaneous compounds The major compounds in Chinese vinegars were furfural, acetic acid, ethyl acetate,

3-hydroxy-2-butanone, 3-methyl-1-butanol, isopentyl acetate, benzaldehyde, phenylethyl alcohol The PCA results showed

that characterizing the Chinese vinegars by HS-SPME-GC-MS was highly related to their type, fermentation method, and

production area, and all these influencing factors were not independent The CA results indicated that the fermentation

method had a greater effect than vinegar type and production area The results showed that HS-SPME-GC-MS together

with chemometrics could provide practical reference for characterization of Chinese vinegars

Keywords: characterization, Chinese vinegar, cluster analysis, headspace solid-phase microextraction, principal component

analysis, volatiles

Practical Application: HS-SPME coupled with GC-MS was applied for the determination of the characteristic volatile

profiles of Chinese vinegars The major compounds in Chinese vinegars were furfural, acetic acid, ethyl acetate,

3-hydroxy-2-butanone, 3-methyl-1-butanol, isopentyl acetate, benzaldehyde, phenylethyl alcohol HS-SPME-GC-MS

together with chemometrics was an efficient tool for evaluating vinegar authenticity

Introduction

Vinegar is consumed worldwide as a food condiment and

preser-vative, especially in the Chinese diet Chinese vinegar has a history

of more than 3000 y (Shi 1999) Over 26 million hectoliters of

vinegar is produced every year, and more than 3.2 million liters

of vinegar is consumed every day in China Nowadays, Chinese

governments pay more and more attention on the quality control

of vinegar (Liu 2010) The aromatic vinegar, mature vinegar, rice

vinegar, and white vinegar are China’s 4 famous types of vinegar

The aromatic vinegar is dark gray or yellowish-brown, lustrous in

color and creamy, aromatic, mildly acidic, tasty, and slightly sweet

in flavor The mature vinegar ranges from brown to dark gray,

lustrous in color with a smoky smell, moderately acidic, and sweet

in flavor The rice vinegar is reddish-pink in color and exhibits a

pleasantly fresh and sweet smell, mildly acidic, slightly tasty, and

MS 20110094 Submitted 1/22/2011, Accepted 7/10/2011 Authors Xiao, Niu,

Yu, Zhu, Tian, and Gu are with School of Perfume and Aroma Technol., Shanghai

Inst of Technol., Shanghai 200233, China Author Dai is with School of Biological

Engineering, East China Univ of Science and Technol., Shanghai 200237, China.

Direct inquiries to author Xiao (E-mail: xzb@sit.edu.cn).

sweet in flavor The white vinegar is yellowish in color, aromatic,and strongly acidic in flavor

In Europe, the discrimination and characterization of gars have been widely investigated using gas chromatography massspectrometry (GC-MS) (Gerbi and others 1997; Tesfaye and oth-ers 2002; Callej ´on and others 2009) In China, several studieswere carried out to analyze Chinese vinegar using gas sensor ar-rays (Zhang and others 2006; Yin and others 2008) The maindifferences between Chinese vinegars and European vinegars areraw materials Chinese vinegars are usually produced from rice,sticky rice, sorghum, and wheat bran, while European vinegarsare mainly fermented from wine, cider, fruit juices, malted bar-ley, honey, and pure alcohol (Mej´ıas and others 2002) Chinesevinegars have a strong regional characteristic For example, Shanxiprovince is famous for mature vinegars and Jiangsu province isfamous for aromatic vinegars (Zhang and others 2006)

vine-Flavor is one of the important factors of vinegar character Theflavor of vinegar depends on the raw materials (rice, sticky rice,wheat bran, sugar, salt, and so on), the constituents formed dur-ing the fermentation and, in some cases, the substances formedduring aging (Cocchi and others 2008) Since the volatile profile

of vinegar represents a fingerprint of the sample, it is assumedthat a discrimination approach based on the analysis of volatile

C

r

Trang 27

Headspace solid-phase microextraction (HS-SPME) is a fast,sensitive, and powerful method which offers large advantages overother sample preparation techniques as it eliminates the use ofextraction solvent and allows the extraction and the concentra-tion steps to be performed simultaneously (Guerrero and others2007) HS-SPME-GC-MS has been successfully used to analyzevolatile compounds from a large variety of food commodities forboth characterization and classification purposes (Wang and oth-ers 2009; Yang and others 2009; Zhao and others 2009; Callej ´onand others 2010; Garc´ıa-Mart´ın and others 2010) Pizarro andothers (2008) applied the HS-SPME-GC-MS and stepwise lineardiscriminant analysis (SLDA) method to classify different types ofEuropean vinegar Cirlini and others (2011) used the HS-SPME-GC-MS and principal component analysis (PCA) and classificationtree (CT) to classify the Balsamic vinegars of Modena (BVM) ofdifferent maturation and aging, and it indicated that this methodwas useful to discriminate BVM samples of different maturationand aging.

In this work, HS-SPME-GC-MS was applied to identify andquantify the volatile compounds in Chinese vinegars Using mul-tivariate analysis tools, such as PCA and cluster analysis (CA),the vinegar samples were characterized according to their type,fermentation method, and production area

Materials and Methods

Vinegar samplesEleven commercial Chinese vinegars were purchased from a lo-cal market in Shanghai, China The samples were kept refrigerated

at 4C Table 1 lists the name, type, raw materials, fermentationmethod, and production area which were copied from the vinegarbottle labels Since geographical discrimination was attempted, theproduction areas are shown in Figure 1

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be more efficient at extracting the volatile compounds of vinegar

than other fibers such as those coated with

polydimethylsilox-ane (PDMS), carbowax-divinylbenzene (CW-DVB), and

poly-dimethyl siloxane-divinylbenzene (PDMS-DVB) In this research,

a manual SPME holder together with one 75 μm

carboxyl-polydimethylsiloxane (CAR-PDMS) fiber, 20 mL vials, and Teflon

covers was used (Supelco Inc., Bellefonte, Pa., U.S.A.) Before

sorption, the fiber was preconditioned for 30 min on the Agilent

6890 gas chromatograph (Agilent Technologies, New York, N.Y.,

U.S.A.) with the injector temperature of 250C Between

injec-tions, the fiber was desorbed for 10 min at 250C in split mode

in order to prevent any contamination

The 20 mL vial with 5 mL Chinese vinegar sample and

20μL internal standard solution (2-octanol [40 mg/L in ethanol],

Sigma-Aldrich, St Louis, Mo., U.S.A.) was sealed up with one

Teflon cover The SPME fiber was exposed in the upper space of

the vial at 45C for 30 min while shaken at intervals, and then

withdrawn and directly introduced to the GC-MS injector for

desorption and analysis

GC-MS

GC-MS analysis was carried out on an Agilent 6890 gas

chro-matograph equipped with a mass selective detector (MSD) model

5973 N (Agilent Technologies) The capillary column used was

an HP-Innowax (60 m × 0.25 mm i.d × 0.25 μm film,

Agi-lent) from Agilent Technologies The injection was conducted in

splitless mode for 3 min at 220C The GC operation conditions

were as follows The injector temperature was 220C; the carrier

gas employed was helium (purity 99.999%) at a constant flow rate

of 1 mL/min The oven temperature was held at 40C for 2 min,

ramped to 150 C at the rate of 3C/min, then again ramped

to 220C at the rate of 5 C/min, and maintained for 5 min

The MSD was used for identification and electron impact energy

was 70 eV The ion source temperature was set at 230C The

quadrupole mass filter was operated at 150C The transfer line

temperature was at 250C The chromatograms were recorded by

monitoring the total ion currents in the 30 to 450 mass range In

terms of the number of peaks and peak area, several parameters in

the chromatogram were adjusted to increase reliability Peak width

was set to 0.04 and initial threshold was set to 13 All samples were

analyzed in triplicate and the average values were calculated

Compound identification and quantification

The volatile compounds were identified by comparing Kovats

retention indices (RI) (Kovats, 1965) and the MS fragmentation

patterns with those of reference compounds, or with mass spectra

in the Wiley7n.l and NIST05 Database (Agilent Technologies)and previously reported Kovats RI The Kovats RI of unknowncompounds were determined via sample injection with a homol-ogous series of alkanes (C6–C25) (Sigma-Aldrich) The GC-MSconditions were the same as described above To quantify thevolatiles, the integrated areas based on the total ion chromatogramswere normalized to the areas of the internal standard The rela-tive volatile concentrations in the 11 samples were determined

by comparison with the concentration of the internal standard(2-octanol)

Multivariate analysisPCA is essentially a descriptive method PCA was used to pro-vide a partial visualization of data in a reduced-dimension plot.The principal components or eigenvectors are orthogonal and theyare a linear combination of the original variables This method,normally the first step in data exploration, allows the main vari-ability aspects of a data set to be visualized without the constraint

of an initial hypothesis concerning the relationship within samplesand between samples and responses (variables) The main goals ofthis method are to find relationships between the different param-eters (objects and variables) and to detect possible clusters withinobjects or/and variables (Garc´ıa-Mart´ın and others 2010)

CA is an unsupervised chemometric technique that revealsthe natural groupings existing between samples characterized bythe values of measured variables A Euclidean metric is used in the

CA with an “average between groups” method of linkage

In this research, PCA was performed on the mean values of therelative volatile concentrations using the correlation matrix with

no rotation CA was employed to examine the relationships of theinfluencing factors (type, fermentation method, and productionarea) of various vinegars more intuitive All statistical analyses wereperformed using XLSTAT ver.7.5 (Addinsoft, New York, N.Y.,U.S.A.)

Results and Discussion

Volatile compounds in Chinese vinegar samplesThe assignments of the principal peaks of Chinese vinegar sam-ples’ volatile profile obtained from HS-SPME-GC-MS analysis areshown in Figure 2 Table 2 lists the identified volatile compounds

in the 11 samples by their chemical classes, relative tions, and RIs on the HP-Innowax column, respectively A total

concentra-of 56 volatile components, including 15 esters, 10 aldehydes, 5acids, 12 alcohols, 5 ketones, 4 volatile phenols, 2 pyrazines, and

3 miscellaneous compounds, were identified Among the fied volatiles, esters, acids, aldehydes, and alcohols were the largest

quanti-Figure 2–The representative total ion chromatogram for volatiles of vinegar sample.

Trang 30

Esters. A total of 15 esters were detected and were among one

of the largest classes of detected compounds The ethyl acetate,isopentyl acetate, phenethyl acetate, and isobutyl acetate were themajor compounds in the 11 samples All the detected esters werepreviously found in various vinegars (Durante and others 2006;Garc´ıa-Mart´ın and others 2010) The content of ethyl acetate inthe type of rice vinegar and white vinegar (except Biaoding Baicu)was much higher than that in the other types of samples Themanufacturing process of rice vinegar and white vinegar employsliquid fermentation rather than solid fermentation The liquidfermentation may affect rice lipid utilization and formation of highmolecular weight esters (Ames and Macleod 1984) Esters werederived from the esterification of free fatty acids and alcohols.Thus, esters of the corresponding fatty acids were expected to bepresent However, the current results showed that some esters wereabsent even though their corresponding fatty acids were found.This could be an indication of either their presence in minuteamount, which was below the detection limit of the analyticalinstrument, or their absence in the process

Aldehydes. Ten aldehydes were identified in the ples, and 5 of them (furfural, benzaldehyde, acetaldehyde, 4-methoxybenzaldehyde, and cinnamaldehyde) were found in all the

sam-11 samples All the compounds were previously detected in variousvinegars (Del Signore 2001; Mar´ın and others 2002; Casale andothers 2006) The most abundant aldehydes in Chinese vinegarswere furfural, with the concentration of 35 mg/L The furfuralconcentrations in the 4 samples (Meigui Micu, Biaoding Baicu,Hengshun Baicu, and Qingfeng Baicu) were much lower thanthose in the other samples The reason could be owed to thedifferent fermentation methods Furans such as furfural and 5-methylfurfural can be formed by sugar dehydration or fragmenta-tion during the Maillard reaction (Fors 1983) Benzaldehyde wasdescribed as having sweet, fruity, nutty, and caramel-like odors

In addition, 4-methoxylbenzaldehyde (also named anisaldehyde)with sweet, powder, and spicy aroma, was the principal constituent

of anise oil (Rodrigues and others 2003) Due to low odor olds and distinctive odors, the above volatile aldehydes are potentialcontributors to Chinese vinegars (Xie and others 2008)

thresh-Acids. Five acids were identified in the samples, including lowcarbon chain saturated acid (C2–C10) The majority of the acids arereleased during extracellular digestion by lipases, while propanoicacid and 3-methylbutanoic acid (isovaleric acid) are consideredbyproducts of yeast protein metabolism (Han and others 2001).Among the 6 acids, the content of acetic acid was the highest.3-Methylbutanoic acid was a combination of milk aroma, souraroma, fruit aroma, and fat aroma It is a key compound in themajority of fermented products like cheese and yogurt (Ohatahand others 2009) Acids, such as hexanoic acid, were absent inthe type of Baicu samples (Biaoding, Hengshun, and Qingfeng).However, high concentrations of corresponding esters (ethyl hex-anoate) were found in these samples Because ethyl esters are

Trang 31

derived from the esterification of free fatty acids and ethanol, their

corresponding fatty acids are expected to be present during the

fermentation process However, the current results indicated that

some fatty acids (lactic acid and octanoic acid) were absent even

though their corresponding esters (ethyl lactate and ethyl

oc-tanoate) were found This could be an indication of strong

es-terification in the processing of fermentation in samples

Alcohols. Alcohols were another large class, containing 12

compounds in the samples Among the alcohols,

3-methyl-1-butanol, 2,3-butanediol, and phenylethyl alcohol were the major

compounds These alcohols were also reported in balsamic vinegar

(Del Signore 2001) and wine vinegar (Morales and others 2004;Callej ´on and others 2010) as important contributors of flavor.Phenylethyl alcohol not only serves as a perfume formulation in-gredient in the flavor industry, but also acts as an aroma enhance-ment in the fermentation products such as bean paste (Lee andAhn 2009) The fusel alcohols, including 2-methylpropanol and3-methylbutanol, were mainly produced by the action of variousfungal enzymes during fermentation (Chung and others 2005).Hexanol, a common and important flavor component for somevegetables and plants, was the key component for compound-ing vegetable flavor It was derived from the bioremediation of

Variables (axes F1 and F2: 55.95 %)

AD1

AD2

AD6 AD7

AD8 AD9 AD10

ES1

ES2

ES3 ES4

ES5 ES6

ES7 ES8

ES9

ES10 ES11

KE4

KE5

AL1 AL2

AL3 AL4

AL5 AL6

PH2 PH3 PH4

by their chemical classes:  , aldehyde (AD);, ester (ES);, ketone (KE);  , alcohol (AL); ♦, acid (AC);◦, pyrazine (PY); +, phenol (PH);

–, miscellaneous (MI).

Observations (axes F1 and F2: 55.95 %)

aro_solid_shang

aro_solid_bei aro_solid_heng aro_solid_zheng

mat_solid_dong mat_solid_jin

ric_solid_jin ric_liquid_mei whi_liquid_biaowhi_liquid_heng

Trang 32

unsaturated fatty acids, and was also the prerequisite chemical for

the formation of long-chain esters (Methven and others 2007)

Ketones. A total of 5 ketones were identified, including 4

aliphatic ketones (2-butanone, 2,3-butanedione, 2-heptanone,

3-hydroxy-2-butanone) and 1 cyclic ketone

(1-phenyl-1-propanone) The concentration of 3-hydroxy-2-butanone in the

vinegar samples, which accounted for approximately 7 mg/L, was

much higher than those other ketones 3-Hydroxy-2-butanone

was a characteristic compound of acetification (Morales and others

2001) 3-Hydroxy-2-butanone was produced during alcoholic

fer-mentation by the action of several microorganisms and was present

in fermented foods and beverages such as wine, vinegar, and

sev-eral dairy products (Caligiani and others 2007) In the QingfengBaicu sample, only 3-hydroxy-2-butanone was detected, lackingmajor ketones such as 2-butanone and 2,3-butanedione Somealiphatic ketones, such as 2-butanone and 2,3-butanedione, could

be products of lipid oxidation or degradation, assisted by enzymesfrom the inoculated mold (Wang and Hesseltine 1970)

Phenols. A total of 4 phenols (4-(1-methylpropyl)-phenol,2-methoxyphenol, 2-methoxy-4-methylphenol, phenol) werefound in the 11 vinegar samples As is well known, phenolswere responsible for smoky and phenolic odors Phenolic com-pounds were mainly produced by thermal degradation throughdepolymerization or oxidation of lignin, which was composed of

Observations (axes F1 and F2: 55.95 %)

whi_liquid_qing

whi_liquid_heng whi_liquid_biao

ric_liquid_mei ric_solid_jin

mat_solid_jin mat_solid_dong

aro_solid_zheng aro_solid_heng aro_solid_bei

Figure 5–PCA results of the vinegar samples;

making for vinegar type:  , aromatic vinegar;+,

mature vinegar;, rice vinegar;, white vinegar.

Observations (axes F1 and F2: 55.95 %)

aro_solid_shang

aro_solid_bei aro_solid_heng aro_solid_zheng

mat_solid_dong mat_solid_jin

ric_solid_jin ric_liquid_mei

Figure 6–PCA results of the vinegar samples;

making for raw material:  , sticky rice;+, neither

rice nor sticky rice;, rice.

Trang 33

repeating phenol units having 3 carbon side chains (Natera and

others 2003) Because of their low threshold value, their flavor

is a characteristic aroma of the vinegars, although the content of

phenols was not very high

Pyrazines. Only 2 pyrazines (trimethylpyrazine and

3-ethyl-2, 5-dimethylpyrazine) were identified in the Chinese vinegars,

which were in relatively low concentration Pyrazine was not

found in the Meigui Micu, Biaoding Baicu, Hengshun Baicu,

and Qingfeng Baicu samples Pyrazines had a mixed aroma of

nut, peanut, and cocoa, particularly alkyl-pyrazines (Gilbertson

and Koenig 1979) In general, although pyrazines were present in

small quantities in natural samples, their contribution to the flavor

of these samples was considerable

Miscellaneous compounds. Three additional miscellaneouscompounds were identified in the 11 samples 2-Acetylfuran waspreviously found in balsamic vinegar (Cocchi and others 2004) and

coffee brews (Lopez-Galilea and others 2006) It was recognized as

having green rice and brown sugar aromas (Fors 1983) Furans can

be formed by sugar dehydration or fragmentation in the Maillardreaction (Fors 1983) Limonene considered to be one of the majorcontributors to orange flavor, had a weak, citrus-like aroma with

a high orthonasal odor threshold (13.7 ppm) in a deodorized

Observations (axes F1 and F2: 55.95 %)

aro_solid_shang

aro_solid_bei aro_solid_heng aro_solid_zheng

mat_solid_dong mat_solid_jin

ric_solid_jin ric_liquid_mei whi_liquid_biao

Observations (axes F1 and F2: 55.95 %)

aro_solid_shang

aro_solid_bei aro_solid_heng aro_solid_zheng

mat_solid_dong mat_solid_jin

ric_solid_jin ric_liquid_mei

Trang 34

orange juice matrix (Plotto and others 2004) Anethole had an

aniselike odor and sweet taste It was a major component in anise

oil and is often used in the alcoholic beverage industry (Chung

and Cadwallader 1994)

Principal component analysis

PCA was used to provide a partial visualization of data in a

reduced-dimension plot Figure 3 and 4 show the first 2

prin-cipal components (PCs) accounted for 55.95% of the total

vari-ation across the samples (PC1 and PC2 accounted for 33.19%

and 18.77% of the variance, respectively) When examining the

volatile distributions (Figure 3), the major compounds positively

contributing to the PC1 dimension (factor loadings> 0.7) were

aldehydes such as acetaldehyde (AD1), 2-methylpropanal (AD2),

5-methylfurfural (AD8), 4-methoxybenzaldehyde (AD9), and

cinnamaldehyde (AD10); esters such as 2-butyl acetate (ES5) and

methyl cinnamate (ES15); ketones such as 2-butanone (KE1),

2,3-butanedione (KE2), and 3-hydroxy-2-butanone (KE4); alcohols

such as 2-butanol (AL1) and furfuryl alcohol (AL9); acids such as

propionic acid (AC2), hexanoic acid (AC5), and trimethylpyrazine

(PY1); phenols such as 2-methoxyphenol (PH2) and

2-methoxy-4-methylphenol (PH3); and miscellaneous compounds such as

limonene (MI1), 2-acetylfuran (MI2), and anethole (MI3) On

the negative side of the PC1 axis, ethyl acetate (ES2) was the main

compound (factor loadings< −0.7) In contrast, the important

compounds of the PC2 dimension were esters such as propyl

acetate (ES4), ethyl hexanoate (ES9), ethyl benzoate (ES12),

and diethyl succinate (ES13); ketones such as 2-heptanone

(KE3) and 1-phenyl-1-propanone (KE5); and alcohols such

as 1-propanol (AL2), 1-pentanol (AL5), and 1-hexanol

(AL6)

It was possible to determine the major volatile compoundscontributing to the differences in the samples by analyzing thecorrelation of each variable (Table 2) with the PC1 and PC2scores (Figure 4) In the upper side of PC1, the Shanghai Xi-angcu sample (aro_solid_shang) was located in the same direc-tion as the esters (ES4, ES9, ES13), ketones (KE3, KE5), andalcohols (AL2, AL5, AL6), which had the highest concentrations

of these compounds among the tested samples Similarly, in thelower right side of PC1, the Donghu Chencu (mat_solid_dong)and Jinbiao Chencu (mat_solid_jin) samples were highlyassociated with aldehydes (AD1, AD2, AD6, AD8, AD9, AD10),ketones (KE1, KE2, KE4), phenols (PH2, PH3), trimethylpyrazine(PY1), and miscellaneous compounds (MI1, MI2) On the nega-tive side of PC1 and on the positive side of PC2, the Jindan Micu(ric_solid_jin), Biaoding Baicu (whi_liquid_biao), and HengshunBaicu (whi_liquid_heng) samples were located in proximity withesters (ES2, ES6, ES8) and 2-methyl-1-propanol (AL3) On thenegative side of PC1 and PC2, the Meigui Micu (ric_liquid_mei)sample was highly associated with ethyl butanoate (ES7) and bu-tanoic acid (AC3)

To discriminate the samples of different types, raw terial, fermentation method, and production area, the samedata were plotted with different markings in Figure 5 to

ma-8, which showed the PCA plots of the vinegars based ontype, raw material, fermentation method, and production area,respectively

It can be observed that 4 distinct groups, which correspond toaromatic vinegar, mature vinegar, rice vinegar, and white vinegar,respectively, are well distinguished in Figure 5 It can be observedthat all the vinegars were well associated to their type, which is acritical factor to the character of Chinese vinegars The aromatic

Figure 9−CA dendrogram based on the

concentration of 56 volatiles to the 11 vinegar samples.

Trang 35

vinegars and the mature vinegars are the most favorite vinegars

in China The aromatic vinegars are fermented from sticky rice

and mainly produced in Jiangsu province, the mature vinegars

are fermented from sorghum and produced in Shanxi province,

while the rice vinegars and white vinegars are fermented from

rice and mainly produced in Shanghai The difference between

the aromatic vinegars and the mature vinegars is big, while the

difference between the rice vinegars and the white vinegars is very

small in Figure 5 The difference between the Shanghai Xiangcu

and the other aromatic vinegars is also big, though they all belong

to the aromatic vinegar type The reason is owed to the different

production areas (Shanghai and Jiangsu province, respectively)

Comparing the relationships between the vinegars and their raw

materials was difficult in this study because each vinegar contained

more than 3 or 4 different materials As shown in Figure 6, the

vinegars can also be clearly divided into 3 groups according to their

main raw material, the samples aro_solid_zheng, aro_solid_bei,

aro_solid_heng, and aro_solid_shang including sticky rice in the

raw material, mat_solid_dong and mat_solid_jin without rice or

sticky rice, and ric_solid_jin, ric_liquid_mei, whi_liquid_biao,

whi_liquid_heng, and whi_liquid_qing made from rice So it is

clearly discernable that the main raw material is an important

factor in characterizing Chinese vinegars

As shown in Figure 7, the vinegars can be clearly divided into

2 groups according to their fermentation methods, solid

fermen-tation vinegar and liquid fermenfermen-tation vinegar The Jindan Micu

(ric_solid_jin), which belongs to the solid fermentation vinegar,

is very close to the group of the liquid fermentation vinegars in

Figure 7 The use of similar raw materials is the possible

rea-son for the small difference between Jindan Micu and the liquid

fermentation vinegars It was concluded that the fermentation

method was highly related to the vinegar raw materials and was

also an essential factor to the character of Chinese vinegars

As shown in Figure 8, the regional definition of the samples

is not that clear compared to type, raw material, or fermentation

method Traditionally, Chinese vinegars have a strong regional

characteristic For example, Shanxi province is famous for mature

vinegars and Jiangsu province is famous for aromatic vinegars The

difference between the Jiangsu vinegars and the Shanghai vinegars

is small, while the difference between the Jiangsu vinegars and the

Shanxi vinegars is very big This phenomenon can be explained

by Jiangsu being very close to Shanghai, but quite far from Shanxi,

indicating that the production area is also an important factor to

character the Chinese vinegars

From the above analysis, it can also be obtained that all the

influencing factors are not independent

Cluster analysis

In the present research, CA was applied to study the relationships

and the scale of the type, fermentation method, and production

area, when the vinegar samples were analyzed by

HS-SPME-GC-MS The similarities between samples were calculated on the basis

of the Euclidean distance and the CA dendrogram is shown in

Figure 9

Two different groups can be observed in the dendrogram

The 1st group included the samples ric_solid_jin, ric_liquid_mei,

whi_liquid_biao, whi_liquid_heng, and whi_liquid_qing, which

referred to rice vinegar and white vinegar except the sample

aro_solid_shang And the samples aro_solid_zheng, aro_solid_bei,

aro_solid_heng, mat_solid_dong, and mat_solid_jin formed the

2nd group, which referred to aromatic vinegar and mature vinegar

This shows that the rice vinegar and white vinegar are

similar, while the aromatic vinegar and the mature vinegar aresimilar The reason for this phenomenon is the same fermenta-tion method, the 1st group and the 2nd group belonged to theliquid fermentation and solid fermentation, respectively The Eu-clidean distance between the aromatic vinegars of aro_solid_zhengand aro_solid_heng is close However, the Shanghai Xiangcu(aro_solid_shang), which also belongs to the aromatic vinegars,

is close to the Jindan Micu (ric_solid_jin) This agrees with thePCA results and the reason has been discussed before Taken as

a whole, these results indicate that the fermentation method is amore important factor than the vinegar type and raw materials ininfluencing the characters of Chinese vinegars

Conclusions

This study represents one of the first approaches to the terization of Chinese vinegars by HS-SPME-GC-MS The resultsobtained from the analysis of the volatile profile of Chinese vine-gars coupled with statistical data analysis by means of PCA and

charac-CA have shown that this method can be useful to characterize ferent Chinese vinegar samples (types, fermentation method, andproduction area), to have a quality and authenticity evaluation ofthe product The volatile profile of Chinese vinegars belonged tothe following families: esters, aldehydes, acids, alcohols, ketones,volatile phenols, pyrazines, and miscellaneous compounds ThePCA results showed that a large number of volatiles corresponded

dif-to each of the Chinese vinegars Aromatic vinegar samples werelocated in the same direction as the alcohols and acids Similarly,mature vinegar samples were highly associated with aldehydes andketones on the positive side of the PC1 axis On the negative side

of PC1 and on the positive side of PC2, rice vinegar and whitevinegar samples were located in proximity with esters It was clearthat characterizing the Chinese vinegars by HS-SPME-GC-MSwas highly related to their type, fermentation method, and produc-tion area, and all these influencing factors were not independent.The CA results showed that the fermentation method was moreimportant than the type and production area Future studies mightexplore more vinegar samples of other varieties and build a morerobust model for the characterization and classification of vinegars

by HS-SPME-GC-MS

Acknowledgments

The authors gratefully acknowledge the financial supportprovided by National Natural Science Foundation of China(nr 20876097) and National 973 Foundation of China (nr2009CB226104)

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Underestimation of Pyruvic Acid

Concentrations by Fructose and Cysteine

in 2,4-Dinitrophenylhydrazine-Mediated

Onion Pungency Test

Kil Sun Yoo, Eun Jin Lee, and Bhimanagouda S Patil

Abstract: Onion pungency has been routinely measured by determining pyruvic acid concentration in onion juice

by reacting with 2,4-dinitrophenylhydrazine (DNPH) since 1961 However, the absorbency of the color adduct of thereaction rapidly decreased in onion samples as compared to that of the pyruvic acid standards, resulting in underestimations

of the pyruvic acid concentrations By measuring the absorbency at 1 min, we have demonstrated that accuracy could besubstantially improved As a continuation, the causes of degradation of the color adduct after the reaction and pyruvic aciditself before the reaction were examined in this study Alliinase action in juice (fresh or cooked) and bulb colors did notinfluence the degradation Some organic acids indigenously found in onion, such as ascorbic acid, proline, and glutamicacid, did not reduce the absorbency However, fructose within the onion juice or supplemented caused the degradation

of the color adduct, whereas sucrose and glucose had a lesser effect Degradation rates increased proportionally as fructoseconcentrations increased up to 70 mg/mL Cysteine was found to degrade the pyruvic acid itself before the pyruvic acidcould react with DNPH Approximately 90% of the pyruvic acid was degraded after 60 min in samples of 7 mM pyruvicacid supplemented with 10 mg/mL cysteine Spectral comparisons of onion juice containing fructose naturally and pyruvicacid solution with supplemented fructose indicated identical patterns and confirmed that the color-adduct degradationwas caused by fructose Our study elucidated that fructose, a major sugar in onion juice, caused the degradation of coloradduct in the onion pungency test and resulted in underestimation of the pyruvic acid concentration

Keywords: cysteine, dinitrophenylhydrazine (DNPH), fructose, pungency, pyruvic acid

Introduction

Onion pungency has been widely measured by reacting

2,4-dinitrophenylhydrazine (DNPH) with the pyruvic acid found

in the onion juice Pyruvic acid is a byproduct of alliinase

hydrolysis of the flavor precursors in onions upon cell disruption

(Schwimmer and Western 1961; Randle and Bussard 1993; Yoo

and others 1995; Boyhan and others 1999; Yoo and Pike 1999;

Anthon and Barret 2003) Though pungency itself is caused by

many sulfur compounds from the alliinase reaction (Lancaster and

Boland 1990), pyruvic acid concentration is linearly proportional

to the levels of S-alk(en)yl-cysteine-sulfoxides, the flavor precursor

compounds (Lee and others 2009) The pungency level of onions

was largely determined by cultivar and secondarily modified by

environmental factors (Yoo and others 2006)

The pungency test method was first introduced by Schwimmer

and Western (1961) and has been modified for faster sample

processing and interference reduction (Randle and Bussard 1993;

Yoo and others 1995; Boyhan and others 1999; Yoo and Pike

1999; Anthon and Barret 2003) However, significant variation

MS 20110146 Submitted 2/2/2011, Accepted 7/7/2011 Authors are with

Veg-etable and Fruit Improvement Center, Dept of Horticultural Sciences, Texas A&M

Univ., College Station, TX 77843 Direct inquiries to author Yoo (E-mail: k-yoo@

tamu.edu).

existed among pyruvic acid test results from various laboratories

of the same source of onions (Havey and others 2002) Previously,our automated method measured approximately 17% higherlevels of pyruvic acid than did the manual spectrophotometricmethod when undiluted juice samples were used (Yoo and others2011) The absorbency of the color adduct rapidly decreased inundiluted onion juice samples as compared to that of the pyruvicacid standards, therefore resulting in underestimations of pyruvicacid concentrations (Yoo and others 2011) In that study, we havemodified the sample processing order and substantially improvedthe consistency by promptly measuring the absorbency at 1 minafter the color development

DNPH has long been used for detection of pyruvic acid andother carbonyl compounds and others by reacting nonselectivelywith carbonyl compounds to form the corresponding hydrazone( Jones and others 1961; Katsuki and others 1961; Schwimmer andWestern 1961; Critchfield 1963) Pyruvic acid andα-ketoglutaric

acid (Katsuki and others 1961), dicarbonyl compounds (Jones andothers 1961), and several aldehydes, such as n-octanal found incitrus (Peleg and Mannheim 1970), have been measured using thismethod In theory, slight overestimations of pyruvic acid contentsare likely due to the coexistence of related carbonyls in onions.Therefore, a high-performance liquid chromatography (HPLC)method was used to very accurately determine the pyruvic acidcontent in onions (Yoo and Pike 2001)

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The addition of NaOH or KOH to pyruvic acid-DNPH

reactions following heating at 37C results in a pink color adduct,

the absorbency of which can be measured spectrophotometrically

(Schwimmer and Western 1961) However, degradation of the

color adduct over time has not been well documented Measuring

the absorbency within 10 min of adding NaOH was

recom-mended and the degradation of DNPH by oxidizing agents was

indicated Ozone can destroy DNPH alone or following formation

of dinitrophenyl- hydrazones during determination of aldehydes

and ketones in the air (Achatz and others 1999) However, further

degradation of the pyruvic acid-DNPH adduct was not

exam-ined (Critchfield 1963) Anthon and Barret (2003) indicated a

2.5% reduction of the color adduct in 1 h and suggested prompt

absorbency measurements We have documented that about 20%

of absorbency was reduced in 60 min, regardless of bulb color

(Yoo and others 2011) However, the cause of the degradation

was not investigated or reported yet to our knowledge

Pyruvic acid is known to be degraded by polymerization and

decomposition in solution (The Merck Index 1991), but this slow

degradation was not noticeable within several hours and was not

regarded as a factor in this study Rather, we were interested in

other factors in onion juice that caused rapid degradation of

pyru-vic acid Only other factor causing degradation of pyrupyru-vic acid was

found to be cysteine that induced coupled oxidation of pyruvic

acid when cysteine was oxidized (Cavallini 1951)

As a continuation of our previous study of observing the rapid

degradation of the color adduct, we initiated this study to elucidate

the cause of color adduct degradation from the reaction of pyruvic

acid and DNPH used in onion pungency tests The reduction of

pyruvic acid concentrations through the addition of cysteine prior

to the reaction with DNPH was also investigated Spectral analysis

of these reactants was performed to confirm the changes in the

color adduct

Materials and Methods

Chemicals and plant materials

All chemicals, unless otherwise stated, were purchased from

Sigma (St Louis, Mo., U.S.A.) NaOH was purchased from Fisher

Scientific (Pittsburgh, Pa., U.S.A.) Red, yellow, and white onion

bulbs of unknown cultivars were purchased from a local store

Onion juice preparation

Fresh juice. The neck, base, and dry skin were removed from

the onion bulbs Bulbs were blended in a mixer for 2 min without

the addition of water The puree was incubated for 30 min at 24C

of room temperature to complete the alliinase reaction and filtered

through P-1 filters (Fisher Scientific) The juice was placed in a

50-mL tube and stored at−20C Frozen samples were defrosted

and centrifuged at 804 g for 30 min to remove particles Onion

juices, unless specified as cooked, refer to the fresh juice in this

study

Cooked juice. The white onion bulb were microwaved for

the rate of 1 min per 100 g tissue, blended, and filtered through a

cheese cloth Filtrates were centrifuged, filtered through P-1 filter

papers, and kept at−20C.

Production of color adduct in the pyruvic acid analysis

We used our previously published pyruvic acid analysis method

to examine undiluted onion juice (Yoo and others 1995) In

this study, the volume of each reactant was reduced to a third

of the originally published volumes to accommodate the use of

1 × 1 × 4.5 cm plastic cuvettes Twenty microliters of luted onion juice, pyruvic acid standard, or other mixtures werecombined in cuvettes with 1-mL DNPH (125 mg/L in 2N HCl)solution using an autodispenser (Hamilton Microlab 500 series,Reno, Nev., U.S.A.) The mixture was incubated in a 37C waterbath for 10 min, and 2-mL NaOH (1.0 N) was added with anEppendorf repetitive pipette Absorbencies at 485 nm weremeasured using a spectrophotometer (Model 601, Milton Roy,Rochester, N.Y., U.S.A.)

undi-Search for factors affecting color adduct degradation

Comparison of fresh and cooked onion juices. Since thealliinase reaction produces many changes in the composition ofonion juice, juice with or without the alliinase reaction was com-pared A white onion bulb (approximately 500 g) was cut in halflongitudinally Half was blended and processed as described in thefresh juice section The other half was microwaved for 2.5 minand processed as described in the cooked juice section

Because the cooked juice contained only approximately0.2 mM pyruvic acid (Yoo and Pike 2001), 38.5 mg sodiumpyruvic acid was dissolved in 50-mL cooked juice in order toobtain pyruvic acid concentrations similar to the 7 mM pyruvicacid standard and fresh juice The final pyruvic acid concentration

in the cooked juice was not measured, but was estimated to bearound 7.2 mM Fresh onion juice had pyruvic acid levels ofapproximately 6 to 7 mM as determined in a separate test Thecooked- and fresh-juice samples and the 7 mM pyruvic acid stan-dard were treated with DNPH as described above Absorbencieswere monitored for 120 min, and relative absorbencies (%, 100×absorbency at a given time/initial absorbency) were calculated

Comparison between bulb colors. Differences in the rates

of color adduct degradation were examined between red, low, and white onions because yellow and red onions containantioxidant compounds, such as quercetin and anthocyanins (Kimand others 2004) Fresh red, yellow, and white onion juices wereassayed as above, and absorbencies were monitored for 60 min.Relative absorbencies were calculated The pyruvic acid concen-trations of the red, yellow, and white onions were 11.8, 3.7, and6.4 mM, respectively

yel-Screening of candidate compounds. Several compoundsthat naturally exist in onion tissues were evaluated for their role

in color adduct degradation A 7 mM pyruvic acid solution wasprepared and 50 mg/mL of ascorbic acid, amino acids (proline,cysteine, and glutamic acid), or sugars (glucose, fructose, andsucrose) were individually dissolved in 10 mL of the pyruvic acidsolution The duplicated samples were analyzed as above, and ab-sorbencies were monitored for 60 min Actual absorbencies arepresented to more clearly represent the reduction of color adductdue to cysteine

The effect of fructose on color adduct degradation

Addition of fructose to various juice mixtures. Solutions

of 7 mM pyruvic acid, fresh or cooked white onion juice, andfresh or cooked white onion juice supplemented with 50 mg/mLfructose were prepared Samples were treated with DNPH, ab-sorbencies were measured for 60 min, and relative absorbencieswere calculated

Fructose concentrations. Solutions of 7 mM pyruvic acidsupplemented with 0 (control), 10, 30, 50, or 70 mg/mL fructosewere prepared Samples were treated with DNPH, absorbencieswere measured over 60 min, and relative absorbencies werecalculated

Trang 39

Comparison of different sugars. The 7 mM pyruvic acid

solution was supplemented with 50 mg/mL fructose, glucose, or

sucrose The control had no sugar added (pyruvic acid alone)

Samples were treated with DNPH, absorbencies were measured

for 60 min, and relative absorbencies were calculated Samples

were prepared in duplicate

The effect of cysteine on absorbencies

Color adduct degradation and cysteine concentrations.

A 7 mM pyruvic acid solution was supplemented with 0, 5, 10,

or 15 mg/mL cysteine Samples were treated with DNPH,

ab-sorbencies were measured for 60 min, and relative abab-sorbencies

were calculated Samples were prepared in duplicate

HPLC measurement of pyruvic acid. The HPLC system

included a binary pump, an autosampler, and a UV/Vis

detec-tor (Perkin Elmer LC 200 Series, Norwalk, Conn., U.S.A.) An

Alltech IOA 100 organic acid column (Deerfield, Ill., U.S.A.,

7.8× 300 mm2) with a guard cartridge was used to separate

pyru-vic acid (Yoo and Pike 2001) The solvent was water containing

0.3-mL sulfuric acid/L at a rate of 0.5-mL/min and a 20-μL

sample was injected The column temperature was 45C, and

de-tection was made at 210 nm External standard of sodium pyruvic

acid ranging from 0 to 5 mM was prepared for a standard curve

It took 30 min to run a sample

A 7 mM pyruvic acid solution was supplemented with

10 mg/mL cysteine and the changes in pyruvic

acidconcentra-tions were measured at 0, 1, 31, 61, and 720 min The peak area at

0 min was measured prior to the addition of cysteine The pyruvic

acid+ cysteine samples were injected into the HPLC system and

peak areas were recorded Relative pyruvic acid concentrations

(%, 100× peak area at a given time/initial peak area) and

regres-sion coefficients were calculated

Spectral analysis of the color adduct

The color adduct developed during the pyruvic acid test

method was placed in a plastic cuvette and the spectrum between

340 and 700 nm was recorded by a spectrophotometer (Model

U-2900, Hitach High-Tech, Schaumburg, Ill., U.S.A.) The

ref-erence control, containing water rather than pyruvic acid, was

used as the background measurement

Comparison of onion juice and the pyruvic acid

standard. Fresh yellow onion juice and 7 mM pyruvic acid

stan-dards were analyzed as described above Their spectra were plotted

on the actual scale and were normalized to overlap the spectra The

λmax was determined and the reference wavelengths used in the

previous papers are indicated

Changes of spectra in the standard and

fructose-supplemented samples. The 7 mM pyruvic acid standard,

cooked white onion juice fortified with 7 mM pyruvic acid

and 50 mg/mL fructose, and 7 mM pyruvic acid fortified with

70 mg/mL fructose were treated with DNPH and the color adduct

developed The spectral data from each sample were collected at

0, 10, and 20 min

Results and Discussion

Effects of alliinase activity and onion color on the

reduction of the color adduct

The color adduct resulting from the pyruvic acid standard was

fairly stable and degraded little over 120 min (Figure 1, left)

How-ever, the color adducts that developed in the reactions containing

fresh juice and cooked juice supplemented with 7 mM pyruvic

acid decreased rapidly The cooked juice samples lost slightly morecolor than the fresh juice samples after 2 h There were no differ-ences in the rates of color reduction in the reactions containingjuice from the different colored onions (Figure 1, right).These results indicated that there was no difference in the coloradduct produced by samples with active or denatured alliinase.Therefore, another factor caused the color adduct degradation inthe onion juice itself Since cooking denatured the alliinase, whichcatalyzes the 1-propenyl-cysteine-sulfoxide and methyl-cysteine-sulfoxide reactions that produce numerous sulfur volatiles and re-lated compounds (Lancaster and Boland 1990), any product fromthose hydrolysis reactions were excluded from the candidate com-pounds There was no retardation or acceleration of the coloradduct degradation by quercetin and anthocyanin compounds,compounds that determine onion bulb colors (Kim and others2004) Red onions contain anthocyanins and quercetin, yellowonions contain quercetin, and white onions do not contain eithertype of compound The onions examined had different colors andpungency levels (3.7 to 11.8 mM), but showed very similar patterns

of reduction Therefore, neither bulb color nor pungency leveleffected the reduction rate of the color adduct Additionally, thio-sulfinates and other sulfur compounds were excluded by this study.Effect of amino acids, sugars, and ascorbic acid on thereduction of the color adduct

The effect of amino acids, sugars, and ascorbic acid on therates of color adduct degradation was examined A 7 mM pyru-vic acid sample was supplemented with 50 mg/mL of proline,cysteine, glutamic acid, ascorbic acid, or fructose and subjected

to the DNPH reaction All samples, including the pyruvic acidcontrol, showed rapid reduction of absorbency between 0 and 5min following the addition of NaOH This reduction was possiblydue to a mixing problem or to an unknown mechanism of initialdegradation (Figure 2) However, there was little linear reduction

of absorbencies between 5 and 60 min, with a total reduction ofless than 6% in 30 min, in all samples except for the fructose-supplemented sample The sample supplemented with fructoseshowed a more rapid reduction in absorbencies over time There-fore, we further studied the effects of fructose on the degradation

of the color adduct Interestingly, cysteine showed a much-reducedinitial absorbency, as compared with the other treatments How-ever, the rate of degradation over time was similar to the othertreatments We suspect that cysteine has some reaction with pyru-vic acid even before the initiation of the DNPH reaction Ascorbicacid at a concentration of 50 mg/mL induced a reduction by 5min, but was not further studied because of its naturally low con-centration in onion (approximately 50μg/mL).

Effect of fructose on the reduction of the color adduct

Addition of fructose to fresh or cooked onion juice. Theabsorbencies of the cooked juice supplemented with 7 mM pyru-vic acid and the fresh juice were reduced by about 20% and 30%after 60 min, respectively (Figure 3) The fresh and cooked juicessupplemented with 50 mg/mL fructose lost about 60% of theirinitial absorbencies in 60 min However, the absorbency of thepyruvic acid alone did not change much There was slightly morereduction of the color adduct (10%) in the cooked juice supple-mented with pyruvic acid than in the fresh juice sample, thoughfructose content was expected to be the same in both samples.The samples supplemented with fructose lost the color adduct

at equal rates These results indicated that higher concentrations

of fructose correlated with higher rates of absorbency reduction

Trang 40

It was estimated that the shortday onion “Texas Grano 1015Y”

contains approximately 20 mg/mL fructose, 23.6 mg/mL glucose,

and 3 mg/mL sucrose (Hamilton and others 1997) Therefore, the

fresh and cooked onion juices used in this study likely contained

about 20 mg/mL fructose and the fructose-fortified juice samples

contained about 70 mg/mL fructose The rates of reduction of

the color adduct absorbencies positively correlated with the

con-centration of fructose in the test samples, thereby demonstrating

that fructose caused the reductions of the color adduct As

com-pared with the Schwimmer and Western method (using 1 mL of

200-fold diluted juice), our method (using 80μL of undiluted

juice) was calculated to contain 16 times more juice (or fructose)

As a result, more rapid absorbency reduction was thought to be

possible

Comparison of fructose concentrations and other

sugars. Pyruvic acid supplemented with 30 or 70 mg/mL

fruc-tose showed 10% and 60% reductions in absorbency, respectively

(Figure 4, left) Color adduct degradation was proportional to

the fructose concentrations As compared to sucrose and glucose,

fructose showed the greatest effect on the absorbencies of the

color adduct (Figure 4, right) There was a 4% to 6% and 7%

to 12% reduction at 30 and 60 min in pyruvic acid samples

supplemented with 50 mg/mL glucose and fructose, respectively

Fructose showed very rapid color reduction of 12% and 38% by

30 and 60 min, respectively

The addition of fructose up to 70 mg/mL to the 7 mM pyruvic

acid sample did not increase the actual absorbency at 485 nm, or

the addition of 50 mg/mL sucrose or glucose, or fructose increased

the absorbency by only 0.010, 0.019, or 0.034 units, respectively

(data not shown) The absorbency of the 7 mM pyruvic acid

was about 0.480 Therefore, the increases in absorbency caused

by sucrose, glucose, and fructose at 50 mg/mL (278 mM) were

insignificant or negligible

Fructose and glucose have a ketone and an aldehyde group,

respectively, and are reducing sugars (The Merck Index 1991)

However, fructose caused an approximately 3-fold greater

degra-dation of the color adduct than did glucose The ketone or

alde-hyde groups in fructose and glucose were believed not to react

with DNPH, because no significant increase in absorbency was

observed Fructose and glucose in solution are mostly in the cyclic

forms of pyranose and furanose (Hyv ¨onen and others 1977; Flood

and others 1996) Therefore, the keto and aldehyde groups in

the acyclic forms were incorporated into the ring structures and

Time after adding NaOH (min)

Control Proline Ascorbic Cysteine Glutamic Fructose

Figure 2–Changes in absorbency measurements of the DNPH-pyruvic acid color adduct in samples of 7 mM pyruvic acid supplemented with

50 mg/mL proline, ascorbic acid, cysteine, glutamic acid, or fructose over

7 mM pyruvate Fresh juice Fresh juice + fructose Cooked juice + pyruvate Cooked juice + pyruvate + fructose

Figure 3–Changes in the relative absorbencies of the DNPH-pyruvic acid color adduct in 7 mM pyruvic acid, fresh or cooked onion juice, and fresh or cooked onion juice supplemented with 50 mg/mL fructose over 60 min.

Time after adding NaOH (min)

Time after adding NaOH (min)

84 86 88 90 92 94 96 98 100

7 mM pyruvate Yellow White Red

Figure 1–Reduction of the relative absorbencies of the DNPH-pyruvic acid color adduct following the addition of NaOH in a 7 mM pyruvic acid standard, fresh onion juice, and cooked onion juice supplemented with 7 mM pyruvate over 120 min (left), and juice samples from yellow, white, or red onions over 60 min (right).

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