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Pecticoligosaccharidesfromagriculturalby-products:production,characterizationandhealthbenefits

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Crit Rev Biotechnol, Early Online: 1–13! 2015 Informa Healthcare USA, Inc. DOI: 10.3109/07388551.2014.996732

REVIEW ARTICLE

Pectic oligosaccharides from agricultural by-products: production,characterization and health benefits

Neha Babbar1,2, Winnie Dejonghe1, Monica Gatti2, Stefano Sforza2, and Elst Kathy1

1Separation & Conversion Technology, VITO-Flemish Institute for Technological Research, Boeretang, Mol, Belgium and 2Department of Food

Science, University of Parma, Parco Area delle Scienze, Parma, Italy

Abstract

Pectin containing agricultural by-products are potential sources of a new class of prebioticsknown as pectic oligosaccharides (POS). In general, pectin is made up of homogalacturonan (HG,a-1,4-linked galacturonic acid monomers) and rhamnogalacturonan (RG, alternate galacturonicacid and rhamnose backbone with neutral side chains). Controlled hydrolysis of pectincontaining agricultural by-products like sugar beet, apple, olive and citrus by chemical,enzymatic and hydrothermal can be used to produce oligo-galacturonides (GalpOS), galacto-oligosaccharides (GalOS), rhamnogalacturonan-oligosaccharides (RGOS), etc. However, extensiveresearch is needed to establish the role of POS, both as a prebiotic as well as therapeutic agent.This review comprehensively covers different facets of POS, including the nature and chemistry ofpectin and POS, potential agricultural residual sources of pectin, pre-treatment methods forfacilitating selective extraction of pectin, identification and characterization of POS, healthbenefits and important applications of POS in food and feed. This review has been compiled toestablish a platform for future research in the purification and characterization of POS and forin vivo and in vitro studies of important POS, so that they could be commercially exploited.

Keywords

Agricultural residues, health benefits,pectic oligosaccharides, pectic substances,prebiotic

History

Received 9 January 2014Revised 12 September 2014Accepted 12 September 2014Published online 2 February 2015

Introduction

Pectin is a complex and heterogeneous polysaccharide present

within the primary cell wall and intercellular regions of higher

plants (Chen et al., 2013). Pectin comprises a family of acidic

polymers, known as homogalacturonan (HG) and rhamnoga-

lacturonan (RG) with several neutral sugars/polymers such as

arabinans, galactans and arabinogalactans (attached as side

chains) (Obro et al., 2004; Strasser & Amado, 2001). The

extraction of these neutral and acidic polymers in the form of

pectic oligosaccharide (POS) is a promising step towards the

manufacture of prebiotics from agricultural by-products

(Munoz et al., 2012; Westphal et al., 2010). Pectic oligosac-

charides (POS) are non-digestible oligosaccharides which

beneficially affect the host by selectively stimulating the

growth and/or activity of one or a limited number of bacteria in

the colon (Bifidobacteria and Lactobacilli) (Baldan et al.,

2003; Garthoff et al., 2010; Gibson & Roberfroid, 1995;

Manderson et al., 2005; Mussatto & Mancilha, 2007;

Roberfroid, 1996). Pectic oligosaccharides have been reported

to suppress the activity of entero-putrefactive and pathogenic

organisms (Baldan et al., 2003; Garthoff et al., 2010; Gibson &

Roberfroid, 1995; Manderson et al., 2005; Mussatto &

Mancilha, 2007; Roberfroid, 1996). The colonic fermentation

of prebiotic POS results in the generation of short-chain fatty

acids (SCFA), which exerts a number of health effects like

inhibition of pathogenic bacteria, relief of constipation,

reduction in blood glucose levels, improvement in mineral

absorption, decreased incidence of colonic cancer and modu-

lation of the immune system (Gullon et al., 2013). The

literature also suggests that POS can act as phytoalexin elicitor,

flowering inducer and antibacterial agent in plants (Iwasaki

et al., 1998).

Agricultural by-products have been studied extensively

for bioethanol production (Brienzo et al., 2009; Oberoi

et al., 2011a), enzyme synthesis (Dhillon et al., 2011; Oberoi

et al., 2012) and protein enriched cattle feed (Laufenberg et al.,

2003). Some agricultural by-products like apple pomace, sugar

beet pulp, berry pomace also contain significant amounts of

pectin (Martinez et al., 2010; Munoz et al., 2012). The

production of POS from these agricultural residues is an

interesting way to reuse waste streams for both environmental

and economic benefits. The most common and well

known POS are arabinogalacto-oligosaccharides, arabinox-

ylo-oligosaccharides, arabino-oligosaccharides, galacto-oligo-

saccharides, oligo-galactouronides and rhamnogalacturonan-

oligosaccharides (Concha-Olmos & Zuniga-Hansen, 2012;

Martinez et al., 2009). This review has been compiled to

provide information on the nature and chemistry of pectin;

potential sources of pectin; various pre-treatment methods

for the production of POS from pectin containing agricultural

by-products; purification and characterization of POS; health

benefits of POS and potential application of these compounds

in food and feed industry.Address for correspondence: Dr Elst Kathy, Tel: +32-14335617. Fax:+32-14321186. E-mail: kathy.elst@vito.be

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Nature and chemistry

Pectin

Pectin is a complex macromolecule made up of several

monosaccharides containing diverse linkages. The structure of

pectin is hypothesized to be made up of ‘‘smooth’’

homogalacturonic (polygalacturonic acid) and branched

‘‘hairy’’ rhamnogalacturonic regions (in which most of the

neutral sugars are located) (Yapo et al., 2007). A schematic

representation of the structure of pectin and the constituent

sugars in each region is presented in Figure 1. Four main pectic

components have been identified, namely, homogalacturonan

(HG), rhamnogalacturonan-I (RG-I), rhamnogalacturonan-II

(RG-II) and xylogalacturonan (XG) (Caffall & Mohnen, 2009;

Gullon et al., 1989; Ralet et al., 2001; Voragen et al., 2009;

Yapo et al., 2007) All these pectic components are connected

by either covalent or ionic cross links (Schols & Voragen,

2002). The most abundant pectic polysaccharide HG is made

of galacturonic acid (Galp) residues with a-1,4-linkages and

comprises more than 65% pectin (Yapo et al., 2007). It can be

partly methyl-esterified at C-6 and possibly partly acetyl

esterified at O-2 and O-3 (Ralet et al., 2001).

The RGI backbone is composed of [!2)-a-L-Rhap-

(1! 4)- a-D-GalpA-(!1] repeats (Westphal et al., 2010).

Rhamnose is a minor component of the pectin backbone and

introduces a kink into the straight chain. The length and

quantity of HG and RG-I components can vary in different

plants (Gullon et al., 2013). For instance, in sugar beet pectin,

the length of HG polymer is shorter than that of pectin of

citrus and apple. On the other hand, RG-I is more abundant in

sugar beet pulp than in citrus and apple (Gullon et al., 2013).

Rhamnogalacturonan I has a number of side chains in the

form of sugars and branched oligosaccharides attached to its

backbone (Willats et al., 2001). The length of these side

chains can vary from single neutral glycosyl to polymeric side

chains of different types viz. (1! 5)-a-L-arabinans, (1! 4)-

b-D-galactans, arabinogalactans-I, arabinogalactans-II (Obro

et al., 2004). Rhamnogalacturonan II is a structurally complex

pectin and accounts for more than 10% pectin (O’Neill et al.,

1990). The building blocks of RG-II are galacturonic acid,

rhamnose, galactose and unusual neutral sugars. The structure

of RG-II is characterized as a distinct region within HG that

contains a cluster of side chains of rare sugar residues, such as

apiose, aceric acid, 3-deoxy-lyxo-2-heptuloasaric (DHA) and

3-deoxy-manno-2-octulosonic acid (Zandleven et al., 2007).

Xylo-galacturonan (XGA) is a substituted HG with a single

unit of b-D-Xylp-(1! 3) side chain (Voragen et al., 2009).

The presence of XGA has been mainly identified in repro-

ductive organs or storage tissues such as in the cell walls of

peas, soybeans, watermelons, apples, pears, onions, potatoes,

pine pollen and cotton seed (Wong, 2008; Zandleven et al.,

2007).

Figure 1. Structure of pectic polysaccharide.

2 N. Babbar et al. Crit Rev Biotechnol, Early Online: 1–13

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Pectin complexes

There are three type of pectin complexes, namely HG calcium,

RG-II borate and uronyl ester complex. The HG calcium

complex is formed by two unesterified HG chains, whereby the

carboxyl groups of two GalpA residues form a negatively

charged pocket that binds with a Ca2+ cation. A minimum of 10

continuous unesterified GalpA residues are needed to build a

stable cross-link between the chains (Vincken et al., 2003).

Calcium cross linking of HG contributes to the cell wall

strength by bringing blocks of unmethylesterified HG chains

into a tightly packed conformation (Caffall & Mohnen, 2009).

The second pectin crosslink is known as the borate diol ester

(RG-II borate). This is formed by two RG-II molecules with

boron. Only the apiofuranosyl residues of the 2-O-methyl-D-

xylose containing side chains in each subunits of the dimer can

participate in the cross-linking. Borate-diol esters can also

crosslink two HG chains as RG-II is an integral part of HG

chain. Cations such as Ca2+ Pb2+, Sr2+ and La3+ promote

dimer formation in vitro (Caffall & Mohnen, 2009).

Homogoalacturonan can also cross-link to other components

by uronyl ester. Approximately 2% of GalpA residues can be

cross-linked this way. Homogalacturonan is mainly found in

plant cell walls in a methyl-esterified form and it is clear that

these molecules hold enormous potential for cross-linking

(Caffall & Mohnen, 2009).

Potential sources of pectic oligosaccharides

Pectin containing by-products, in addition to their conven-

tional uses, can also be exploited for POS production. Table 1

illustrates the quantity of pectin rich agricultural by-products

produced in Europe along with the content of HG and RG

sugars. Further, Table 2 gives a detail insight of the pectin

content as well as acidic and neutral sugar composition of

important agricultural by-products.

Olive (Olea europaea) pomace

Olive pomace is the by-product of olive oil processing. Spain is

the leading producer of olive oil in the world. The production of

olive oil generates huge quantities of olive pomace. Cell wall

material from olive pomace comprises a number of molecular

components, with considerable quantities of pectic polysac-

charides (39%), cellulose (30%), hemicellulosic polymers rich

in xylans and glucuronoxylans (14%), xyloglucans (15%) and

mannans (2%) (Jimenez et al., 1994, 2001).

The pectic polysaccharides of olive pomace are unique due

to the presence of arabinan. The degree of methyl esterifica-

tion and acetylation in olive pomace was determined to be 48

and 11%, respectively, by Cardoso et al (Cardoso et al., 2003)

which suggests high gelling properties of pectin. Due to

high arabinan and galacturonic acid, olive pomace can be

considered as a potential source of POS (Coimbra et al., 2010;

Munoz et al., 2012; Rodrı́guez et al., 2007). Hydrothermal

processing of olive pomace has been reported to produce

tetra-, tri- and di-galacturonic acid and different structures of

neutral and acidic xylo-oligosaccharides (Munoz et al., 2012).

Sugar beet (Beta vulgaris) pulp

Sugar beet pulp is a by-product of the sugar refining industry

and is used mostly as animal feed. It is combined with

molasses and dried to give a high energy feed for ruminants.

Sugar beet pulp polysaccharides consist approximately of

22–24% cellulose, 30% hemicellulose, 15–25% pectin, 3% ash

and 5.9% lignin (Sun & Hughes, 1999). Beet pulp contains

low amounts of protein, lignin and fat. The combination of

shorter HG chain length, high degree of acetylation and the

higher concentration of side chains (containing neutral sugars)

contributes to the poor gelling properties of sugar beet pectin.

Production of POS from sugar beet pulp (SBP) has been

successfully carried out by various researchers (Concha-

Olmos & Zuniga-Hansen, 2012; Leijdekkers et al., 2013).

Al-Tamimi et al. (2006) isolated sugar beet arabinan (MW

5700–10 000 Da) and arabino-oligosaccharides from sugar

beet pulp. Kuhnel et al. (2010) characterized branched

arabino-oligosaccharides [having an a-(1,5)-linked backbone

of L-arabinosyl residues] from sugar beet pulp produced by a

mixture of arabinohydrolases.

Table 1. Pectin content and side chain composition of agricultural by-products.

% Total pectin

SourceTotal production

(tones)aPectin

content (%) HG RG I NSC RG II References

Citrus waste 8.0� 104b 30 77 5 4 0.3 (Martinez et al., 2010; Eurostat, 2012;El-Nawawi & Shehata, 1987)

Apple pulp 3.8� 105c 20.9 36 1 47 10 (Voragen et al., 2009; Kołodziejczyket al., 2007; Schemin et al., 2005)

Sugar beet pulp 9.1� 107 16.2 29 4 48 4 (Yapo et al., 2007; Voragen et al., 2009;Faostat, 2012; Guillon et al., 1989)

Olive pomace 1.6� 106d 34.4 – – 38.8 – (Coimbra et al., 2010; Faostat, 2012)Potato pulp 1.3� 105e 15 20 75 – – (Eurostat, 2012; Turquis et al., 1999)Soy hull – 16.31 – – – – (Monsoor & Proctor, 2001)Onion skin 8.5� 104f 27–34 – – – – (Eurostat, 2012; Alexander & Sulebele,

1973)

HG, Homogalacturonan; RG, Rhamnogalacturonan; NSC, Neutral side chainsaWaste statistics Europe, on wet basis.bLemon peels (sum of waste produced during lemon juice and lemon jam processing).cPulp produced during apple juice processing.dPomace produced during olive oil production.ePotato peel (Sum of waste produced during steaming, drying, cutting and slicing.fSum of waste produced during processing of dried onions, whole, cut, sliced, broken.

DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 3

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Potato (Solanum tuberosum) pulp

Potato pulp is a by-product of the potato industry. Potato pulp

consists of pectic polysaccharides (56%), starch (12%),

proteins (5%), ash (4%) fat (0.3 %) and water (9%). The

pectin of potato pulp contains a high proportion of RG-I with

long galactan side chains (75%) (Khodaei & Karboune, 2013;

Thomassen & Meyer, 2010). Previous studies have reported

successful extraction of HG and RG-I oligosaccharides from

potato pulp (Byg et al., 2012; Thomassen et al., 2011). The

RG-I in potato pulp contains a complex arabinogalactan

structure which can be converted to POS (Obro et al., 2004).

Citrus waste

Citrus fruits are the most important fruits grown and

consumed all over the world (Aggarwal & Sandhu, 2004).

The waste from the orange juice processing industry ranges

between 40–60% of the fruit weight and is made up of peel

and segment membranes (Grohmann & Baldwin, 1992).

Citrus reticulata, an important tropical crop, contains 10%

cellulose, 4.28% hemicellulose, 0.56% lignin, 5.78% protein,

22.6% pectin and 3.23% ash (Oberoi et al., 2011b). The

presence of low lignin makes citrus by-products ideal for use

in the area of bioprocessing. Some information on POS

production has been reported in orange peel wastes (Martinez

et al., 2010). Cancalon (1992) found significant amounts of

oligosaccharides of DP42 in naturally fermented citrus

juices. The presence of transfructosidase activity (present in

invertases) catalyses the synthesis of various oligosaccharides

during such fermentations. Kang et al. (2009) evaluated the

positive effects of POS produced by irradiation (10 kGy/h)

from citrus pectin on levels of serum triglyceride, total

cholesterol and LDL-cholesterol in the blood of mice fed

high-cholesterol diets.

Apple (Malus domestica) pomace

Apple pomace a by-product of the apple processing industry

(Watt et al., 1999) accounts for 25–35% of the dry mass of an

apple (Gullon et al., 2007b). It contains 7% protein, 1.4% ash,

8.3% pectin, 58.3% neutral polysaccharides (cellulose and

hemicellulose) (Voragen et al., 2009). The residue of apple

contains highly branched RG and XG polysaccharide (Schols

et al., 1995). These polysaccharides can be further degraded

to produce oligomers of desired chain length. Watt et al.

(1999) and Renard et al. (1995b) obtained fucogalactoxylo-

glucan oligosaccharides from apple pomace by alkaline pre-

treatment. Gullon et al. (2007a) found 32–45% of alcohol

soluble compounds in apple pomace (inclusive of monosac-

charides, oligosaccharides and malic acid). Oligosaccharides

were mainly present in the form of gluco-oligosaccharides,

xylo-oligosaccharides and arabino-oligosaccharides.

Others

Oligo-galacturonic acid (DP 6–12) from tomato processing

waste isolated by acid hydrolysis was found to be potent plant

growth promoter (Suzuki et al., 2002). Hydrolysis of

Lucerene (Medicago sativa) led to the production of acidic

oligosaccharides (Aspinall et al., 1968). Montella et al. (2013)

isolated galacto-oligosaccharides and xyloglucans from hazel

nut skin by alkaline and water extraction. Bilberries and black

currants, important crops in Scandinavian countries contain

pectin. Due to the formation of pectin gel after mashing, some

pectinolytic enzymes are added to the mash to release the

juice. After degradation, some polysaccharides remain in the

mash in the form of RG-II which can be used for POS

production (Hilz et al., 2006). Zykwinska et al. (2008)

obtained POS of different molecular weight from chicory

roots, citrus peel, cauliflower floret/leaves and sugar beet

pulp. Pectic oligomers obtained by hydrolyzing the soybean

polysaccharides were of RG origin (Nakamura et al., 2002).

Cello-oligosaccharides (cellopentaose, cellotetraose, cello-

triose and cellobiose) and galactooligosaccharides (galactote-

traose, galactotriose) from carrot pomace were obtained after

alkaline pre-treatment (Yoon et al., 2005).

Processes for the production of pecticoligosaccharides

Pectic polysaccharides are covalently cross linked and

therefore certain pre-treatment is required to separate HG,

RG-I and RG-II from each other. Pectic oligosaccharides can

be obtained by depolymerization of suitable raw materials by

different pre-treatment methods viz. enzymatic, chemical and

physical (Byun et al., 2006; Chen et al., 2013; Combo et al.,

2012; Martinez et al., 2009). Table 3 comprehensively covers

different pre-treatment approaches for the extraction of POS

from different agricultural by-products.

Table 2. Pectic polysaccharide composition of agricultural by-products.

Source GalpA Ara Rha Fuc Man Xyl Gal References

Orange peela 31 7.78 – – – 4.29 7.47 (Martinez et al., 2010)Chicory roota 23.2 7.2 1.4 0.3 1.7 3.3 3.9 (Zykwinska et al., 2008)Citrus peela 25.8 8.4 0.9 0.6 3 3.7 6.4 (Zykwinska et al., 2008)Cauliflowera,b 16 7.5 1 0.4 1.2 2.4 4.3 (Zykwinska et al., 2008)Endive pulpa 20 8.4 1.2 0.2 1.6 2.5 5.0 (Zykwinska et al., 2008)Beet pulpa 25 22.5 1.6 0.2 1.4 1.9 5.4 (Zykwinska et al., 2008)Apple pulpc 61.1 3.2 4.6 – – 2.7 16.0 (Bonin et al., 2002)Limec 82.3 5.1 5.1 – – 0.2 7.5 (Bonin et al., 2002)Soy hullc 68.72 – – – – – – (Monsoor & Proctor, 2001)Grape skinc 15.4 7.0 1.1 0.1 0.4 1.1 7.5 (Lecas & Brillquet, 1994)

a% dry matter.bCauliflower florets and buds.c% pectin.GalpA, Galacturonic acid; Ara, Arabinose; Rha, Rhamnose; Fuc, Fucose; Man, Mannose; Xyl, Xylose; Gal, Galactose.

4 N. Babbar et al. Crit Rev Biotechnol, Early Online: 1–13

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se)

16

hat

37� C

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ectc

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uct

ura

lin

form

atio

nw

ith

MS

–(C

oen

enet

al.,

20

08

)

Po

ly-g

alac

turo

nic

acid

(mo

del

)E

nz

(EP

G-M

2,

Pec

tin

ase,

Vis

cozy

me

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tin

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tin

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,p

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.8–

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ectc

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cati

on

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hO

lig

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erst

and

ard

s(d

i-an

dtr

i-P

GA

)E

PG

-M2

,2

h:

58

%(w

/w)

DP

31

8%

(w/w

)D

P2

13

%(w

/w)

DP

1o

fto

tal

po

lysa

cch

arid

es

(Co

mb

oet

al.,

20

12

)

Po

lygal

actu

ron

icac

id(m

od

el)

Hy

dro

ther

mal

45

3–

53

3K

at1

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Pa

––

Mix

ture

DP

2–

10

(Miy

azaw

a&

Fu

naz

uk

uri

,2

00

4)

aS

emi-

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dby-p

rod

uct

of

vir

gin

oli

ve

oil

pro

cess

ing

.bP

H,

Po

st-h

yd

roly

sis

(Qu

anti

fica

tio

no

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ead

dit

ion

alm

on

om

ers

form

edby

po

st-h

yd

roly

zin

gth

em

ixtu

re).

cD

irec

t,D

irec

tqu

anti

fica

tio

n/i

den

tifi

cati

on

of

the

oli

go

mer

sp

rese

nt

inth

em

ixtu

re.

Ara

f,ar

abin

ofu

ran

osi

das

e;A

bn

,ar

abin

ohy

dro

lase

;A

OS

,ar

abin

o-o

lig

osa

cch

arid

es;

DH

PM

,d

yn

amic

hig

hp

ress

ure

mic

rofl

uid

izat

ion

;D

P,d

egre

eo

fp

oly

mer

izat

ion

;E

A,en

do

-ara

bin

ase;

En

z,en

zym

atic

;E

nd

oP

G,

end

op

oly

gal

actu

ron

ase;

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A,

exo

-ara

bin

ase;

GO

,g

luco

-oli

go

sacc

har

ides

;G

alO

,gal

acto

-oli

go

sacc

har

ides

;G

alac

idO

,gal

actu

ron

icac

ido

lig

osa

cch

arid

es;

HN

O3,

nit

ric

acid

;M

HR

,m

od

ifie

dh

airy

reg

ion

s;M

S,

mas

ssp

ectr

om

eter

;M

W,

mo

lecu

lar

wei

gh

t;P

OS

,p

ecti

co

lig

osa

cch

arid

e;P

GA

,p

oly

gal

actu

ron

icac

id;

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,rh

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ogal

actu

ron

ase;

SB

P,

sugar

bee

tp

ulp

;X

G,

xylo

gal

actu

ron

an

DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 5

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Enzymatic processes

Various enzymes have been widely used for the production of

POS because of their specificity and selectivity. In addition, the

use of enzymes over other pre-treatment methods is regarded

as safe due to minimum adverse chemical modifications of

products (Kim & Rajapakse, 2005). Some specific pectin

degrading enzymes have been used, which acts synergistically

to produce POS (Combo et al., 2012; Concha-Olmos &

Zuniga-Hansen, 2012; Mandalari et al., 2007; Martinez et al.,

2009; Pedrolli et al., 2012; Voragen et al., 2009). Pedrolli et al.

(2012) reviewed the type of enzymes needed for the production

of POS. Figure 2 illustrates various pectic enzymes active on

smooth and hairy regions of pectin. The methyl esters and

acetyl groups from galacturonic acid residues are removed by

pectin methyl esterase (PME) and pectin acetyl esterase (PAE),

respectively (Shevchik & Hugouvieux, 1997). Both enzymes

act before endo-polygalacturonase (Endo-PG). Endo-polyga-

lacturonase (endo-PG) is able to cleave the glycosidic bond of

the a-(1! 4)-polygalacturonan in a random fashion (Cameron

et al., 2009). Endo-polygalacturonase generally prefers a non-

esterified substrate and shows decreasing activity with

an increasing degree of methyl esterification (Parenicova

et al., 2000). Exo-polygalacturonase (Exo-PG) attacks the

substrate from the non-reducing end and is able to remove

terminally (1-) linked Gal A residues from HG chains (Kester

et al., 1999).

The RG subunit of the ramified ‘‘hairy’’ regions can be

degraded sequentially by rhamnogalacturonan hydrolase (RG),

and rhamnogalacturonanlyase (RGL) both acting on a-D-1,4-

GalpA-a-L-1,2-Rhap and a-L-1,2-Rhap-a-D-1,4-GalpA link-

age of the RG backbone, respectively. Rhamnogalacturonan

acetyl esterase (RGAE) is an exo-acting pectinase active on the

acetyl groups and also removes terminal rhamnosyl residues

(Mutter et al., 1994). The removal of side chains from RGI can

be achieved by a cocktail of various enzymes such as: (i)

arabinofuranosidase B (Araf), which removes terminal arabin-

ose residues from the arabinan side-chains of pectins

(Westphal et al., 2010), (ii) endoarabinase (EA) hydrolyze

the linear regions of the arabinan backbone and release a

mixture of arabinose oligomers (Beldman et al., 1997) (iii)

exoarabinases (ExA) releases arabinose, arabinobiose

(Carapito et al., 2009), arabinotriose (Kaji & Shimokawa,

1984) to from linear a-linked arabinan. These enzymes act in a

synergistic fashion, leading to a rapid degradation of the

arabinans. On the other hand, the relatively long (1! 4)-linked

galactan side-chains can be degraded by endogalactanase

while, b-galactosidase is able to remove terminal galactose

residues from galactans or arabinogalactans (Pedrolli et al.,

2012). Eight neutral branched arabino-oligosaccharides

(a-1,5-linked backbone of L-arabinofuranosyl residues) from

sugar beet arabinan was obtained by a mixture of arabinohy-

drolases, abn 1 (endo-arabinase), abn2 (exo-arabinase) and abn

4 (arabinofuranosidase) (Westphal et al., 2010). Holck et al.

(2011) separated sugar beet pectin into HG and RG-I by

sequentially applying enzymes viz. pectin lyase, b-galactosi-

dase-1, b-galactosidase-2, galactanase, arabinofuranosidase

and arabinanase.

The process parameters, such as time, temperature,

enzyme concentration, absence and presence of particular

enzyme influence oligosaccharides production (Martinez

et al., 2009). Leijdekkers et al. (2013) and Kuhnel et al.

(2010) concluded that branched arabino-oligosaccharides can

be produced if the enzyme mixture lacks arabinofuranosidase.

Same authors observed that the higher enzyme loadings

results in increased arabinan conversion to arabinose. The

presence of galacturonic acid and low DP oligomers indicated

the presence of Exo-PG which cleaves the polygalacturonic

acid oligomers (Combo et al., 2012; Leijdekkers et al., 2013).

The absence of RG rhamnohydrolase and RG galacturonase

led to the production of recalcitrant oligosaccharides

(Leijdekkers et al., 2013) while the presence of rhamnoga-

lacturonase resulted in the production of rhamnogalacturonan

oligomers (Renard et al., 1995b). Feruloylated arabinose di,

tri, hexa, hepta and octa saccharides, as well as feruloylated

galactose disaccharides, were obtained after the hydrolysis of

sugar beet pulp with driselase (Colquhoun et al., 1994). Potato

pulp was hydrolyzed with pectin lyase, polygalacturonase and

Figure 2. Mode of action of differentenzymes on pectin moiety. PME, Pectinmethylesterase; PAE, Pectinacetyl esterase;PG, Polygalacturanase; RGL,Rhamnogalacturonanlyasc; RGAE,Rhamnogalacturonan acetyl esterase; RG,Rhamnogalacturonan hydrolase; AF,Arabinofuraosidase; EA, Endo-arabinase;Endo-Gal, Endo-galactanase; bGal,b-Galactosidase.

6 N. Babbar et al. Crit Rev Biotechnol, Early Online: 1–13

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pectin methyl esterase for the production of HG and RG-I

oligosaccharides (Thomassen et al., 2011).

Physical and chemical processes

For POS production, physical pre-treatments like hydrother-

mal, dynamic high pressure microfluidization (DHPM)

and irradiation have been tried. During hydrothermal pre-

treatment, pectin is partially hydrolyzed and oligosaccharides

can be effectively released from the biomass. Arabino and

galacto-oligosaccharides were successfully produced from

various agro-residues (Gomez et al., 2013; Martinez et al.,

2009; Munoz et al., 2012; Takano & Sato, 2010) by

hydrothermal hydrolysis. Another physical pre-treatment

DHPM, which is based on the principal of powerful shear,

turbulence, impaction and cavitation, has been used for POS

production from apple pectin (Chen et al., 2013). Various DP

of POS were obtained and identified as oligo-galacturonides,

arabino-oligosaccharides and galacto-oligosaccharides.

Chemical hydrolysis of pectin for the production of POS

has not been studied extensively except for the alkaline pre-

treatment which is generally used for the production of RG-I

pectin (Sila et al., 2009). Zykwinska et al. (2006) used

alkaline extraction for the production of RG-I oligosacchar-

ides from potato pulp. There are some disadvantages of

chemical hydrolysis processes, as these are generally not safe

for the environment and there is also a limitation to achieve

the desired degree of polymerization (Kim & Rajapakse,

2005).

Characterization and purification of POS

As mentioned previously, pectin is often pre-treated to

produce POS of varying DPs (Table 3). The effect of this

degradation results in fragments which are in the range of a

broad set of analytical techniques (Schols & Voragen, 2002),

ranging from liquid chromatography, to capillary electrophor-

esis (CE), gas chromatography (GC) and mass spectrometry

(MS). Liquid chromatographic analyses are the most com-

monly used and are often conducted using high performance

anion exchange chromatography with pulsed amperometric

detection (HPAEC-PAD). Sugar oligosaccharides are sepa-

rated based on their charge differences with HPAEC, with the

separation being performed at pH 12. The negatively charged

sugars bind to the column and elute through competitive

binding with an increasing salt gradient (Kabel et al., 2001;

Lee, 1996). A series of galacturonic acid oligomers (DP1–

DP10), formed by depolymerization of polygalacturonic acid,

were identified on HPAEC-PAD (Combo et al., 2012).

Another possibility recently receiving more and more atten-

tion is the use of hydrophilic interaction liquid chromatog-

raphy (HILIC). POS oligomers have recently been efficiently

separated, identified and quantified using HILIC with online

electrospray ionization ion trap mass spectrometry (ESI-IT-

MSn) and evaporative light scattering detection (ELSD)

(Remoroza et al., 2014). The molecular weight of POS can

also be estimated with size exclusion chromatography (SEC)

(Combo et al., 2013). The presence of tetra-, tri- and di-

galacturonic acid, prepared from olive by-products, were

confirmed by adsorption/SEC and identified by HPLC, GC,

ESI-MS and ESI-MS/MS (Munoz et al., 2012). Beside

chromatography, matrix-assisted laser desorption ionization

mass spectrometry, due to its tolerance to residual salts, ease

of simple sample preparation and the high speed of analysis,

is often used for offline MS analysis in order to identify the

DP and the composition of the separated oligomers (Daas

et al., 1998). Arabino-oligosaccharides prepared from sugar

beet pulp were identified by MALDI-TOF MS and HPAEC-

PAD (Westphal et al., 2010).

Purification of POS can be accomplished by membrane

based separation or other chromatography based purification

techniques described elsewhere in this article (Garna et al.,

2006; Leijdekkers et al., 2013). Holck et al. (2011) employed

a regenerated cellulose membrane of 3 kDa molecular weight

cut-off for POS purification. Munoz et al. (2012) obtained

POS by ultrafiltration through 1000, 3000, 5000 and 10 000

Da cellulose regenerated molecular weight cut-off mem-

branes. Different techniques based either on the membrane

based technology or those based on chromatography are

employed for separation of POS of different DPs. It is

important to select the membrane and its cut-off on the basis

of molecular weight of a specific compound. Similarly, the

chemistry of the resin/matrix used during chromatography is

important for separation of a specific POS of a desired DP. In

brief, the separation and purification techniques are generally

chosen according to the compound/mixture of compounds to

be separated from a mixture.

Health benefits of POS

The health effects imparted by oligosaccharides make them

active ingredients of ‘‘functional foods’’ which are similar in

appearance to conventional foods that are consumed as part of

a normal diet and have physiological benefits and/or reduce the

risk of chronic disease beyond basic nutritional functions

(Clydesdale, 1997). As food ingredients, prebiotics have an

acceptable odor and are low-calorie, this allows their utiliza-

tion in anti-obesity diets. It has been stated that the prebiotic

effect of POS depends upon the molecular weight of the

fractions (Chen et al., 2013; Garna et al., 2006). Olano-Martin

et al. (2002) were the first to compare the effect of pectin and

POS on the growth of pure cultures of various species

indigenous to the gastrointestinal tract. Several authors have

reported that low molecular weight POS have a prebiotic

potential better than high molecular weight POS (Al-Tamimi

et al., 2006). In vitro studies have given a clear indication that

POS can be successfully used to promote bifidogenic flora.

Pectic oligosaccharides of DP 3–7 were produced enzymati-

cally from bergamot peel and successfully evaluated for their

prebiotic properties in fecal batch cultures (Mandalari et al.,

2007). Chen et al. (2013) used apple pectin POS and found a

decrease in the number of Bacteroides and Clostridia. The

fermentative capability of some intestinal strains viz.

Bacteroides, Bifidobacterium, Clostridium, Klebsiella and

E. coli was tested on POS prepared from soy arabinogalactur-

onan, sugar beet arabinan, wheat flour arabinoxylan, poly-

galacturonan and rhamnogalacturonan fraction from apple.

Except for Bacteroides, all other species were able to ferment

in vitro (Van Laere et al., 2000). Small oligomers of

galacturonic acid (with DP 2–7) were responsible for inhibiting

the adherence of bacteria to epithelial cells, the initial and

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crucial stage of infection (Guggenbichler et al., 1997). The

in vitro fermentability of apple pomace oligosaccharides

showed an increase in short-chain fatty acids and increased

bacterial growth (Gullon et al., 2011). Holck et al. (2011)

reported that the long-chain arabino-oligosaccharides from

sugar beet pulp have a large bifidiogenic effect in comparison

to short-chain arabino-oligosaccharides. An increase in

Eubacterium rectale population and butyrate levels was

observed with the use of orange peel POS (Manderson et al.,

2005). A stimulation of Bifidobacteria and Lactobacilli

population was seen with the use of low molecular weight

arabino-oligosaccharides (Al-Tamimi et al., 2006).

Pectic oligosaccharides have also been shown to possess

antioxidant activity (Kang et al., 2006) and have a significant

effect lowering the serum levels of total cholesterol (p50.01)

and triglycerides (p50.05) and the inhibition in the accumu-

lation of body fat (Li et al., 2010). Pectic oligosaccharides have

been reported to protect against cardiovascular diseases in vivo

(Li et al., 2010). Treatment with haw POS at higher doses

(150–300 mg/kg) significantly suppressed weight gain in mice

(Li et al., 2010). Little literature is available on the evaluation

of POS isolated from agro-residues for their health benefits.

Table 4 summarizes the biological and prebiotic effects of POS

from agro-processing residues. There have been reports that

POS regulates lipid and glucose metabolism with decreased

glycemic response and blood cholesterol levels (Garna et al.,

2006). Pectic derived acidic oligosaccharides (pAOS) have

been evaluated for their genotoxic potential and the safety of

pAOS for human consumption was tested by Garthoff et al.

(2010). An increase in Bifidobacteria populations and a

considerable decrease in the Clostridium lituseburense/

Clostridium histolyticum group was observed in HIV patients

after ingesting a mixture of POS (Gori et al., 2011).

Other health promoting effects of POS are the protection of

colonic cells against Shigella toxins (Hotchkiss et al., 2003;

Olano-Martin et al., 2003a), prevention of adhesion of

uropathogenic microorganisms (Guggenbichler et al., 1997)

and the stimulation of apoptosis of human colonic adenocar-

cinoma cells (Olano-Martin et al., 2003b). In vivo, the

synergistic empowerment of immunomodulation caused by

galacto-oligosaccharides (GalOS) and fructo-oligosaccharides

(FOS) was studied by Vos et al. (2007). Makker et al. (2002)

have reported inhibition of tumor growth and metastasis by

galactan oligomers. Anti-tumor activity of the galacturonide

(1 kDa) oligosaccharide, obtained from citrus pectin, was

successfully tested on mouse and human tumor cells (Makker

et al., 2002). However, a precise study on the effect of individual

arabino-oligomer, galacto-oligomer, arabino-oligomer is lack-

ing, because POS are generally produced in a mixture and the

complex nature of POSs makes them difficult to separate.

The disadvantages of in vitro methods are the absence of

synergistic, antagonistic, and/or competitive effects as well as

the absence of an immune system. In the field of prebiotics,

POS are an exciting new development as they can be

manufactured from low cost agricultural by-products.

POS in the food industry

Information on the prebiotic activity of POS stated above is

mainly from in vitro models representing the human colon.

However, the mechanisms operating in vivo need to be

elucidated to interpret if these studies can be extended to

human needs as well. Worldwide awareness of consumers

towards diet and health has opened new opportunities for food

industries in research and development of functional foods.

Foods that contain pre- and pro-biotics are drawing the

special attention of consumers and are a potentially exciting

component of the food market. Different prebiotics can be

used for the fortification of different food products to design

functional foods for special target groups. Moreover, pre-

biotics from other sources have been successfully tested for

their stability at high temperature and low pH and can

therefore be added to bakery product, pasteurized juices and

acidic foods like yogurts (Charalampopoulous & Rastall,

2012). The importance of prebiotic foods lies in their active

stimulation of growth of beneficial bacteria, thereby adding

to potential health and nutritional benefits (Panesar et al.,

2014). However, to further substantiate the claim of the

prebiotic efficacy and other health benefits of POS, more

rigorous in vitro investigations are required and in vivo studies

will validate the claim. Potential applications of pre-

biotics (both the food and the non-food) in general are

listed in Figure 3.

POS in the feed industry

As antibiotics are prohibited in many countries due to transfer

of the genes which resists anti-microbial/antibiotic action

from animal to human microbiota (Mathur & Singh, 2005).

Consequently, an alternative is needed that could enhance the

natural defense mechanisms of animals. Poultry flocks are the

main infection sources of Camphylobacter jejuni (Corry &

Atabay, 2001), Clostridia and Salmonella infections. Pigs

have been found to be more prone to E. coli infections.

Oligosaccharides have been found to prevent this kind of

invasion by binding to the microbe’s carbohydrate-binding

proteins and pathogens are cleared by the physiological

mechanism characteristic of the specific tissue (Choct, 2009;

Crittenden, 2006; Zopf & Roth, 1996). In addition, in diets

containing reasonable quantities of carbohydrates, sacchar-

olytic fermentation prevails, thus the pH of the GIT remains

stable and subsequently reduces the onset of Clostridia

infections, as a more alkaline pH is required by species of

this genus. Inulin, added to rabbit feed, was fermented in the

caecum produced SCFA, and reduced the risk of clostridiosis

(Maertens et al., 2004). Pectic oligosaccharides are reported

to possess this activity and have been tested against some

pathogens or toxins (Olano-Martin et al., 2003a). Ganan et al.

(2010) found that POS significantly inhibits cell invasion.

Gaggia et al. (2010) have reviewed, in detail, the application

of prebiotics in animal feeding. As mentioned previously,

there are a number of reports available on the application of

POS in food and pharmaceutical industry. However, their

potential in the feed industry is yet to be exploited. There is

only limited information available on the use of POS in

animal feeds to promote the health of the animal or acting as

therapeutic agents. In vitro studies show that POS have a

potential to be used as feed additives. However, extensive

in vivo studies may be required in different animal models due

to the complex structure of the GIT and diverse microflora.

8 N. Babbar et al. Crit Rev Biotechnol, Early Online: 1–13

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Tab

le4

.H

ealt

hb

enef

its

of

PO

Sex

trac

ted

fro

md

iffe

ren

tso

urc

es.

So

urc

e/T

yp

eo

fP

OS

Eff

ecti

ve

DP

/Mo

lecu

lar

wei

gh

tIn

vivo

/in

vitr

oef

fect

sE

nu

mer

atio

no

fb

acte

rial

gro

wth

/oth

ers

SC

FA

pro

du

ced

/oth

ers

Ref

eren

ces

Ora

nge

pee

lM

ixtu

reo

fP

OS

Bif

ido

ba

cter

ium

and

Eu

ba

cter

ium

rect

ale

aF

luo

resc

ence

insi

tuhy

bri

diz

atio

nL

acti

c,p

rop

ion

ic,

bu

tyri

cb,

Ace

tic

(Man

der

son

etal

.,2

00

5)

Su

gar

bee

tc2

–1

0an

d7

–1

4(B

ifid

ob

act

eriu

m,

Ba

cter

oid

s,L

act

ob

aci

lli)

a,

Clo

stri

dia

dF

luo

resc

ence

insi

tuhy

bri

diz

atio

nA

ceta

tese

and

pro

pio

nat

esf

(Al-

Tam

imi

etal

.,2

00

6)

Po

tato

pu

lp1

0–

10

0K

Dag

;41

00

KD

ah(B

ifid

ob

act

eriu

man

dL

act

ob

aci

lli)

a–

–(T

ho

mas

sen

etal

.,2

01

1)

Ber

gam

ot

pee

l1

40

0–

17

00

KD

a(B

ifid

ob

act

eriu

m,

La

cto

ba

cill

i,E

ub

act

eria

)aan

dC

lost

rid

iab

Flu

ore

scen

cein

situ

hy

bri

diz

atio

n–

(Man

dal

ari

etal

.,2

00

7)

Ara

Gal

OS

fro

mS

oy

–A

ssim

ilat

ion

of

Bac

tero

ides

––

(Ola

no

-Mar

tin

etal

.,2

00

2)

PO

Sfr

om

haw

pec

tin

–D

ecre

ased

seru

mch

ole

ster

ol,

inh

ibit

ion

of

accu

mu

lati

on

of

bo

dy

fat

––

(Kan

get

al.,

20

06

)

Mix

ture

of

PO

S–

Bif

ido

ba

cter

ium

gro

wth

inH

IVp

atie

nts

,re

du

ctio

nin

feca

lp

ath

ogen

s

––

(Li

etal

.,2

01

0)

Aci

dic

(gal

actu

ron

icac

id)

PO

S–

Imp

roved

imm

un

ere

spo

nse

––

(Ola

no

-Mar

tin

etal

.,2

00

3b

)A

cid

ic(g

alac

turo

nic

acid

)P

OS

–R

edu

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DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 9

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Market demand of prebiotics

According to the Global Industry Analysts (GIA) report, the

European and the US market for prebiotics is projected to

reach $1.17 billion and $225.31 million, respectively, by the

year 2015. While the European market is driven by the

expansion of prebiotic ingredient manufacturers into new

application areas such as meat and snack products, the US

market is driven by continued demand for fructans, which

includes both inulin as well as fructo-oligosaccharides. The

global market for prebiotics is projected to reach US$4.8

billion by 2018, driven by the rising awareness of health and

nutrition, growing consumer acceptance of the benefits of

prebiotics, expanding applications and rapid innovations in

prebiotics based food products. The potential in the world

market for emerging prebiotics in terms of their production

and purification is yet to be completely realized and can be

optimized from cellulosic and pectic biomass pre-treatments.

Fructans represent the largest product market worldwide.

Prominence of GOS (Galacto oligosaccharides) is growing

led by the inherent benefits offered by this class of

oligosaccharides in their versatility for use in a wide range

of products including clear beverages, juices and bakery

products. Since pectic oligosaccharides are not yet commer-

cial, it is difficult to predict their contribution to the prebiotic

industry in economic terms. However, it is felt that the POS

are likely to contribute significantly to the prebiotic market in

the years to come. Development of POS from relatively

cheaper by-products such as agro-residues for application in

food, feed and pharmaceutical industry will set new directions

for future research.

Concluding remarks

Hopefully, this review has thrown light on some of the

important aspects of POS and their beneficial effects on

human health. Pectic oligosaccharides belong to an important

category of prebiotics which are also known for prevention

and treatment of various chronic diseases, such as constipa-

tion, hepatic encephalopathy, cancer etc. However, to improve

the economics of prebiotic production, technologies based on

bio-utilization of agro-residues need to be further strength-

ened. In addition, the characterization and purification of

individual oligosaccharide from POS needs further studies to

confirm which POS is responsible for the prebiotic effect and

other health benefits in humans as well as animals. Thus, POS

could be valuable in the development of nutritional and drug

therapies to combat different health ailments. At this stage, it

is also important to conduct extensive research on the

application of POS as biopreservatives, natural therapeutics

and immune building molecules. Their contribution in feeds

which have a direct impact on the quantity and quality of meat

needs extensive research.

Declaration of interest

Authors have no conflict of interest. The authors acknowledge

the work supported by European commission (NOSHAN,

contract no. 312140 FP7 and RESFOOD, contract no. 308316

FP7).

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DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 13

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