Seediscussions,stats,andauthorprofilesforthispublicationat:http://www.researchgate.net/publication/271709831
Pecticoligosaccharidesfromagriculturalby-products:production,characterizationandhealthbenefits
ARTICLEinCRITICALREVIEWSINBIOTECHNOLOGY·FEBRUARY2015
ImpactFactor:7.18·DOI:10.3109/07388551.2014.996732·Source:PubMed
READS
180
5AUTHORS,INCLUDING:
WinnieDejonghe
FlemishInstituteforTechnologicalResearch
63PUBLICATIONS1,061CITATIONS
SEEPROFILE
MonicaGatti
UniversitàdeglistudidiParma
67PUBLICATIONS1,769CITATIONS
SEEPROFILE
KathyElst
FlemishInstituteforTechnologicalResearch
33PUBLICATIONS460CITATIONS
SEEPROFILE
Allin-textreferencesunderlinedinbluearelinkedtopublicationsonResearchGate,
lettingyouaccessandreadthemimmediately.
Availablefrom:NehaBabbar
Retrievedon:06November2015
http://informahealthcare.com/btyISSN: 0738-8551 (print), 1549-7801 (electronic)
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: [email protected]
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
Tab
le3
.D
iffe
ren
tp
re-t
reat
men
tm
eth
od
s,qu
anti
fica
tio
n,
iden
tifi
cati
on
and
yie
ldo
fP
OS
fro
mv
ario
us
agri
cult
ura
lby
-pro
du
cts.
Pre
-tre
atm
ent
Qu
anti
fica
tio
no
fo
lig
osa
cch
arid
es
Su
bst
rate
Ty
pe
Co
nd
itio
ns
Ty
pe
Met
ho
dY
ield
Ref
eren
ces
Alp
eru
joa
Ste
am1
5m
inat
17
0� C
PH
(Aci
d)b
PH
(En
z)b
2N
TF
Aat
12
1� C
for
2h
Oli
vex
�at
40� C
,p
H5
.0fo
r2
4h
23
%(w
/w)
PO
So
fto
tal
po
ly-
sacc
har
ides
(30
00
–1
00
0D
a)(M
un
oz
etal
.,2
01
2)
Ora
nge
pee
lH
yd
roth
erm
al2
88
min
at1
60� C
PH
(En
z)b
Vis
cozy
me
L–
45
U/g
,C
ellu
lase
-5
FP
U/g
45
h,
37� C
,p
H5
25
.1%
(w/w
)P
OS
of
oven
dri
edra
wm
ater
ial.
(Mar
tin
ezet
al.,
20
10
)
Su
gar
bee
tp
ulp
Hy
dro
ther
mal
28
7m
inat
16
0� C
;3
57
min
at1
63� C
PH
(En
z)b
Vis
cozy
me
L–
45
U/g
40
h,
37� C
,p
H5
31
.2%
(w/w
)P
OS
29
.9%
(w/w
)P
OS
of
oven
dri
edS
BP
(Mar
tin
ezet
al.,
20
09
)
Su
gar
bee
tp
ulp
En
z(V
isco
zym
eL
,P
ecti
nas
ean
dco
mb
inat
ion
s)
45� C
up
to4
8h
PH
(Aci
d)b
1h
,3
0� C
in7
2%
(w/w
)H
2S
O4,
foll
ow
edby
3h
,1
00� C
in1
MH
2S
O4.
–(L
eijd
ekk
ers
etal
.,2
01
3)
Su
gar
bee
tA
rab
inan
En
z(A
raf,
Ab
nan
dm
ixtu
res)
–P
H(A
cid
)b
Dir
ectc
1h
,3
0� C
in7
2%
(w/w
)H
2S
O4
foll
ow
edby
3h
,1
00� C
in1
MH
2S
O4;
Qu
anti
fica
tio
nby
arab
ino
seo
lig
om
ers
Mix
ture
so
fD
P1
–6
dep
end
ing
on
con
dit
ion
s(K
uh
nel
etal
.,2
01
0)
Cit
rus
pec
tin
Irra
dia
tio
n1
0k
Gy
/hat
14� C
––
–(K
ang
etal
.,2
00
9)
Pec
tin
(ap
ple
,su
gar
bee
tan
dci
tru
s)A
cid
(HC
l0
.1M
)7
2h
at8
0� C
Dir
ectc
PH
(Aci
d)b
MW
asse
ssm
ent
by
oli
go
gal
ac-
turo
nid
esan
dm
alto
dex
trin
so
f9
80
–1
63
0D
3h
,1
20� C
in2
MT
FA
DP
6–
20
(Ren
ard
etal
.,1
99
5a)
XG
,P
GA
,A
pp
leM
HR
En
z(X
G:
XG
hy
dro
lase
,P
GA
:E
nd
o-P
G,
app
leM
HR
:R
Gh
yd
rola
se)
16
hat
37� C
Dir
ectc
Str
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
L,
Pec
tin
exu
ltra
SP
-L,
Pec
tin
ex6
2L
,M
acer
8F
J)
35
–4
0� C
,p
H3
.8–
5.0
Dir
ectc
Iden
tifi
cati
on
wit
hO
lig
om
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
0M
Pa
––
Mix
ture
DP
2–
10
(Miy
azaw
a&
Fu
naz
uk
uri
,2
00
4)
aS
emi-
soli
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
fth
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;
Ex
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;
RG
,rh
amn
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
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 7
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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
ced
alle
rgic
asth
ma,
(Bif
ido
ba
cter
ium
and
La
cto
ba
cill
i)a,
Clo
stri
dia
b
––
(Mag
ne
etal
.,2
00
8)
Su
gar
bee
tA
rab
inan
2–
10
(Bra
nch
edan
dL
inea
r)(L
act
ob
aci
lli
and
Bif
ido
ba
cter
ium
)aQ
uan
tita
tive
real
-tim
eP
CR
Ace
tate
,p
rop
ion
ate
and
bu
tyra
te(V
igsn
aes
etal
.,2
01
1)
Pec
tin
DP
5an
d9
i ;D
P5
j ;D
P1
0k;
DP
5l
Neu
tral
sug
arfr
acti
on
s:In
crea
sein
gro
wth
of
Bif
ido
ba
cter
ium
;–
–(O
nu
mp
aiet
al.,
20
11
)
Cit
rus
pec
tin
m1
KD
a(O
lig
ogal
actu
ron
ides
)G
row
thin
hib
itio
no
fh
um
anca
nce
rce
lls
––
(Hu
ang
etal
.,2
01
2)
DP
,D
egre
eo
fp
oly
mer
izat
ion
;P
OS
,P
ecti
cO
lig
osa
cch
arid
es;
SC
FA
,S
ho
rt-c
hai
nfa
tty
acid
s.aIn
crea
sein
nu
mb
ers.
bH
igh
est
pro
du
ctio
n.
cF
erulo
yla
ted
and
non-f
erulo
lyla
ted
arab
ino-o
ligosa
cchar
ides
.dD
ecre
ase
inn
um
ber
s.eIn
crea
sed
wit
hd
ecre
asin
gm
ole
cula
rw
eig
ht.
f Dec
reas
edw
ith
dec
reas
ing
mo
lecu
lar
wei
gh
t.gH
om
ogal
actu
ron
an.
hb-
1,4
gal
acta
nch
ain
so
fR
ham
no
gal
actu
ron
an.
i Oli
go
gal
actu
ron
ides
.j M
ethy
late
dO
lig
orh
amn
ogal
actu
ron
ides
.kO
lig
orh
amn
ogal
actu
ron
ides
.l O
lig
ogal
acto
sid
es.
mK
Da,
Kil
oD
alto
n.
DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 9
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
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).
References
Aggarwal P, Sandhu KS. (2004). Effect of hydrocolloids on the quality ofKinnow squash. J Food Sci Technol, 41, 14–21.
Alexander MM, Sulebele GA. (1973). Pectic substances in onion andgarlic skins. J Sci Food Agric, 24, 611–15.
Al-Tamimi MAHM, Palframan RJ, Cooper JM, et al. (2006). In vitrofermentation of sugarbeet arabinan and arabino-oligosaccharides bythe human gut microflora. J Appl Microbiol, 100, 407–14.
Aspinall GO, Gestetner B, Molloy JA, et al. (1968). Pectic substancesfrom lucerne (Medicago sativa). Part II. Acidic oligosaccharides frompartial hydrolysis of leaf and stem pectic acids. J Chem Soc C,2554–9.
Baldan B, Bertoldo A, Navazio L, et al. (2003). Oligogalacturonide-induced changes in the developmental pattern of Daucus carota L.somatic embryos. Plant Sci, 165, 337–48.
Beldman G, Schols HA, Pitson SM, et al. (1997). Arabinans andarabinan degrading enzymes. In: Sturgeon R, ed. Advances inmacromolecular carbohydrate research. vol. 1. London: JAI PressInc.; 1–64.
Bonin E, Dolo E, Goff AL, et al. (2002). Characterisation of pectinsubunits released by an optimized combination of enzymes.Carbohydr Res, 337, 1687–96.
Figure 3. Potential applications of prebiotics.
10 N. Babbar et al. Crit Rev Biotechnol, Early Online: 1–13
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
Brienzo M, Siqueira AF, Milagres AMF, et al. (2009). Search foroptimum conditions of sugarcane bagasse hemicellulose extraction.Biochem Eng J, 46, 199–204.
Byg I, Diaz J, Ogendal LH, et al. (2012). Large-scale extraction ofrhamnogalacturonan I from potato waste. Food Chem, 131, 1207–16.
Byun MW, Kang HJ, Jo C, et al. (2006). Antioxidant and cancer cellproliferation inhibition of citrus pectin-oligosaccharide prepared byirradiation. J Med Food, 9, 313–20.
Caffall KH, Mohnen D. (2009). The structure, function and biosynthesisof plant cell wall pectic polysaccharides. Carbohydr Res, 344,1879–900.
Cameron RG, Luzio G, Savary BJ, et al. (2009). Digestion patterns oftwo commercial endopolygalacturonases on polygalacturonate oligo-mers with a degree of polymerization of 7 to 21. Proc Flu State HurtSoc, 122, 295–302.
Cancalon PF. (1992). Comparison of oligosaccharides generated duringsucrose conversion and citrus juice fermentation. Proc Fla State HortSoc, 105, 160–2.
Carapito R, Imberty A, Jeltsch JM, et al. (2009). Molecular basis ofarabinobio-hydrolase activity in phytopathogenic fungi crystal struc-ture and catalytic mechanism of Fusarium graminearum GH93 exo-a-L-arabinanase. J Biol Chem, 284, 12285–96.
Cardoso SM, Coimbra MA, Silva JAL, et al. (2003). Calcium-mediatedgelation of an olive pomace pectic extract. Carbohydr Polym, 52,125–33.
Charalampopoulous D, Rastall RA. (2012). Prebiotics in foods. CurrOpin Biotechnol, 23, 187–91.
Chen J, Liang RH, Liu W, et al. (2013). Pectic-oligosaccharides preparedby dynamic high-pressure microfluidization and their in vitro fer-mentation properties. Carbohydr Polym, 91, 175–82.
Choct M. (2009). Managing gut health through nutrition. Br Poultry Sci,50, 9–15.
Clydesdale F. (1997). A proposal for the establishment of scien-tific criteria for health claims for functional foods. Nutr Rev, 55,413–22.
Coenen GJ, Kabel MA, Schols HA, et al. (2008). CE-MS of complexpectin-derived oligomers. Electrophoresis, 29, 2101–11.
Coimbra MA, Cardoso SM, Lopes-da-Silva JA, et al. (2010). Olivepomace, a source for valuable arabinan-rich pectic polysaccharides.Chem Mat Sci, 294, 129–41.
Colquhoun IJ, Ralet MC, Thibault JF, et al. (1994). Structure identifi-cation of feruloylated oligosaccharides from sugar-beet pulp by NMRspectroscopy. Carbohydr Res, 263, 243–56.
Combo AMM, Aguedo M, Goffin D, et al. (2012). Enzymatic productionof pectic oligosaccharides with commercial pectinase preparations.Food Bioprod Process, 90, 588–96.
Combo AMM, Aguedo M, Quievy N, et al. (2013). Characterization ofsugar beet pectic-derived oligosaccharides obtained by enzymatichydrolysis. Int J Biol Macromol, 52, 148–56.
Concha-Olmos J, Zuniga-Hansen ME. (2012). Enzymatic depolymer-ization of sugarbeet pulp: production and characterization of pectinand pectic-oligosaccharides as a potential source for functionalcarbohydrates. Chem Eng J, 192, 29–36.
Corry JEL, Atabay HI. (2001). Poultry as a source of Campylobacter andrelated organisms. J Appl Microbiol, 90, 96S–114S.
Crittenden R. (2006). Emerging prebiotic carbohydrates. In: Gibson GR,Rastall RA, eds. Prebiotics development and applications. Chichester(UK): Wiley.
Daas PJH, Arisz PW, Schols HA, et al. (1998). Analysis of partiallymethyl-esterified galacturonic acid oligomers by high-performanceanion-exchange chromatography and matrix-assisted laser desorptionionization time-of-flight mass spectrometry. Anal Biochem, 257,195–202.
Dhillon GC, Oberoi HS, Kaur S, et al. (2011). Value-addition ofagricultural wastes for augmented cellulase and xylanase productionthrough solid-state fermentation employing mixed-culture of fungi.Ind Crops Prod, 34, 1160–7.
El-Nawawi SA, Shehata FR. (1987). Extraction of pectin from Egyptianorange peel. extraction conditions on the yield, purity and surfaceproperties of sugar beet pulp. Factors affecting the extraction. BiolWastes, 20, 281–90.
Eurostat. (2012). Prodcom Annual sold (Nace rev. 2.). www.ec.europa.eu.
Faostat. (2012). Food balance sheets. Commodity balances. Cropsprimary equivalent. Database. www.faostat.fao.org.
Gaggia F, Mattarelli P, Biavati B, et al. (2010). Probiotics and prebioticsin animal feeding for safe food production. Int J Food Microbiol, 141,S15–28.
Ganan M, Collins M, Rastall R, et al. (2010). Inhibition by pecticoligosaccharides of the invasion of undifferentiated and differentiatedCaco-2 cells by Campylobacter jejuni. Int J Food Microbiol, 137,181–5.
Garna H, Mabon N, Nott K, et al. (2006). Kinetics of the hydrolysis ofpectin galacturonic acid chains and quantification by ionic chroma-tography. Food Chem, 96, 477–84.
Garthoff JA, Heemskerk S, Hempenius RA, et al. (2010). Safetyevaluation of pectin-derived acidic oligosaccharides (pAOS): geno-toxicity and sub-chronic studies. Regulatory Toxicol Pharmacol, 57,31–42.
Gibson GR, Roberfroid MB. (1995). Dietary modulation of the humancolonic microbiota-introducing the concept of prebiotics. J Nutr, 125,1401–12.
Gomez B, Gullon B, Yanez R, et al. (2013). Pectic-oligosaccharides fromlemon peel wastes: production, purification and chemical character-ization. J Agric Food Chem, 61, 10043–53.
Gori A, Rizzardini G, Van T, et al. (2011). Specific prebiotics modulategut microbiota and immune activation in HAART-naive HIV-infectedadults: results of the ‘‘COPA’’ pilot randomized trial. MucosalImmunol, 4, 554–63.
Grohmann K, Baldwin EA. (1992). Hydrolysis of orange peel withpectinase and cellulase enzymes. Biotechnol Lett, 14, 1169–74.
Guggenbichler JP, Jurenitsch J, de Bettignies-Dutz A, et al. (1997).Blocking the accumulation of germs on human cells (PCT/EP94/03006). Anticancer Res, 23, 341–6.
Guillon F, Thibault JF, Rombouts FM, et al. (1989). Enzymic hydrolysisof the ‘‘‘hairy’’ fragments of sugar-beet pectins. Carbohydr Res, 190,97–108.
Gullon B, Falque E, Alonso JL, et al. (2007a). Evaluation of applepomace as a raw material for alternative applications in foodindustries. Food Technol Biotechnol, 45, 426–33.
Gullon B, Garrote G, Alonso JL, et al. (2007b). Production of L-lacticacid and oligomeric compounds from apple pomace by simultaneoussaccharification and fermentation: a response surface methodologyassessment. J Agric Food Chem, 55, 5580–7.
Gullon B, Gomez M, Martinez SR, et al. (2013). Pectic-oligosacchar-ides: manufacture and functional properties. Trends Food Sci Technol,30, 153–61.
Gullon B, Gullon P, Sanz Y, et al. (2011). Prebiotic potential of a refinedproduct containing pectic oligosaccharides. LWT Food Sci Technol,44, 1687–96.
Gullon F, Thibault JF, Rombouts FM, et al. (1989). Enzymic hydrolysisof the ‘‘hairy’’ fragments of sugar-beet pectins. Carbohydr Res, 190,97–108.
Hilz H, Williams P, Doco T, et al. (2006). The pectic polysacchariderhamnogalacturonan II is present as a dimer in pectic populations ofbilberries and black currants in muro and in juice. Carbohydr Polym,65, 521–8.
Holck J, Lorentzen A, Vigsnæs LK, et al. (2011). Feruloylated andnonferuloylated arabino-oligosaccharides from sugar beet pectinselectively stimulate the growth of Bifidobacterium spp. in humanfecal in vitro fermentations. J Agric Food Chem, 59, 6511–19.
Hotchkiss AT, Olano Martin E, Grace WE, et al. (2003). Pecticoligosaccharides as prebiotics. In: Eggleston G, Cote G, eds.Oligosaccharides in food and agriculture [Chapter 5]. ACSSymposium Series. Washington (DC): American Chemical Society;54–62.
Huang PH, Fu LC, Huang CS, et al. (2012). The uptake ofoligogalacturonide and its effect on growth inhibition, lactatedehydrogenase activity and galactin-3 release of human cancer cells.Food Chem, 132, 1987–95.
Iwasaki KI, Inoue M, Matsubaro Y, et al. (1998). Continuous hydrolysisof pectate by immobilized endo-polygalacturonase in a continuouslystirred reactor. Biosci Biotechnol Biochem, 62, 262–72.
Jimenez A, Guillen R, Fernandez BJ, et al. (1994). Cell wall compositionof olives. J Food Sci, 59, 1192–201.
Jimenez A, Rodriguez R, Fernandez-Caro I, et al. (2001). Olive fruit cellwall degradation of cellulosic and hemicellulosic polysaccharidesduring ripening. J Agric Food Chem, 49, 2008–13.
Kabel MA, Schols HA, Voragen AGJ, et al. (2001). Mass determinationof oligosaccharides by matrix-assisted laser desorption/ionization
DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 11
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
time-of-flight mass spectrophotometry following HPLC, assisted byon-line desalting and automated sample handling. Carbohydr Polym,44, 161–5.
Kaji A, Shimokawa K. (1984). New exo-type arabinase from Erwiniacarotovara IAM1024. Agric Biol Chem Tokyo, 48, 67–72.
Kang HJ, Jo C, Kwon JH, et al. (2006). Antioxidant and cancer cellproliferation inhibition effect of citrus pectin-oligosaccharides pre-pared by irradiation. J Med Food, 9, 313–20.
Kang HJ, Kwon JH, Ahn DU, et al. (2009). Effect of citrus pectinoligosaccharides prepared by irradiation on high cholesterol dietB6.KOR-APOE mice. Food Sci Biotechnol, 884–8.
Kester HCM, Magaud D, Roy C, et al. (1999). Performance of selectedmicrobial pectinases on synthetic monomethyl esterified di- and tri-galacturonates. J Biol Chem, 274, 37053–9.
Khodaei N, Karboune S. (2013). Extraction and structural characteriza-tion of rhamnogalacturonan I-type pectic polysaccharides from potatocell wall. Food Chem, 139, 617–23.
Kim SK, Rajapakse N. (2005). Enzymatic production and bio-logical activities of chitosan oligosaccharides. Carbohydr Polym, 62,357–68.
Kołodziejczyk K, Markowski J, Kosmala M, et al. (2007). Apple pomaceas a potential source of nutraceutical products. Polish J Food Nutr Sci,57, 291–5.
Kuhnel S, Hinz SWA, Pouvreau L, et al. (2010). Chrysosporiumlucknowense arabinohydrolasees effectively degrade sugarbeet arabi-nan. Bioresour Technol, 101, 8300–7.
Laufenberg G, Kunz B, Nystroem M, et al. (2003). Transformation ofvegetable waste into value added products: (A) the upgradingconcept; (B) practical implementations. Bioresour Technol, 87,167–98.
Lecas M, Brillquet JM. (1994). Cell wall composition of grape berryskins. Phytochemistry, 35, 1241–3.
Lee YC. (1996). Carbohydrate analysis with high-performance anion-exchange chromatography. J Chromatogr A, 720, 137–49.
Leijdekkers AGM, Bink JPM, Geuthes S, et al. (2013). Enzymaticsaccharification of sugarbeet pulp for the production of galacturonicacid and arabinose; a study on the impact of the formation ofrecalcitrant oligosaccharides. Bioresour Technol, 128, 518–25.
Li T, Li S, Du L, et al. (2010). Effects of haw pectic oligosaccharide onlipid metabolism and oxidative stress in experimental hyperlipidemiamice induced by high- fat diet. Food Chem, 121, 1010–13.
Maertens L, Aerts J, De Boever J, et al. (2004). Degradation of dietaryoligofructose and inulin in the gastro-intestinal tract of the rabbit andthe effects on caecal pH and volatile fatty acids. World Rabbit Sci, 12,235–46.
Magne F, Hachelaf W, Suau A, et al. (2008). Effects on fecal microbiotaof dietary and acidic oligosaccharides in children during partialformula feeding. J Pediatr Gastroenterol Nutr, 46, 580–8.
Makker NP, Hogan V, Honjo Y, et al. (2002). Inhibition of human cancercell growth and metastasis in nude mice by oral intake of modifiedcitrus pectin. J Natl Cancer Inst, 94, 1854–62.
Mandalari G, Nueno PC, Tuohy K, et al. (2007). In vitro evaluationof the prebiotic activity of a pectic oligosaccharide-rich extractenzymatically derived from bergamot peel. Appl MicrobiolBiotechnol, 73, 1173–9.
Manderson K, Pinart M, Tuohy KM, et al. (2005). In Vitro determinationof prebiotic properties of oligosaccharides derived from an orangejuice manufacturing by-product stream. Appl Environ Microbiol, 71,8383–9.
Martinez M, Gullon HA, Schols HA, et al. (2009). Assessment of theproduction of oligomeric compounds from sugarbeet pulp. Ind EngChem Res, 48, 4681–7.
Martinez M, Yanez R, Alonso JL, et al. (2010). Chemical production ofpectic oligosaccharides from orange peel wastes. Ind Eng Chem Res,49, 8470–6.
Mathur S, Singh R. (2005). Antibiotic resistance in food lactic acidbacteria – a review. Int J Food Microbiol, 105, 281–95.
Miyazawa T, Funazukuri T. (2004). Hydrothermal production of mono(galacturonic acid) and the oligomers from poly (galacturonic acid)with water under pressure. Ind Eng Chem Res, 43, 2310–14.
Monsoor MA, Proctor A. (2001). Preparation and functional propertiesof soy hull pectin. JAOCS, 78, 709–13.
Montella R, Coisson JD, Travaglia F, et al. (2013). Identification andcharacterisation of water and alkali soluble oligosaccharides fromhazelnut skin (Corylus avellana L.). Food Chem, 15, 717–25.
Munoz AL, Gutierrez GR, Senent FR, et al. (2012). Production,characterization and isolation of neutral and pectic oligosaccharideswith low molecular weights from olive by-products thermally treated.Food Hydrocolloids, 28, 92–104.
Mussatto SI, Mancilha IM. (2007). Non-digestible oligosaccharides: areview. Carbohydr Polym, 68, 587–97.
Mutter M, Beldman G, Schols HA, et al. (1994). Rhamnogalacturonan-L-rhamnopyranohydrolase: a novel enzyme specific for the terminalnonreducing rhamnosyl unit in rhamnogalacturonan regions of pectin.Plant Physiol, 106, 241–50.
Nakamura A, Furuta H, Maeda H, et al. (2002). Analysis of themolecular construction of xylogalacturonan isolated from solublesoybean polysaccharides. Biosci Biotechnol Biochem, 66, 1155–8.
O’Neill M, Albersheim P, Darvill A, et al. (1990). The pecticpolysaccharides of primary cell walls. In: Dey PM, ed. Methods inplant biochemistry. 2nd ed. London: Academic Press; 415–41.
Oberoi HS, Babbar N, Sandhu SK, et al. (2011a). Ethanol produc-tion from alkali-treated rice straw via simultaneoussaccharification and fermentation using newly isolated thermotolerantstrain of Pichia kudriavzevii HOP-1. J Ind Microbiol Biotechnol, 39,557–66.
Oberoi HS, Sandhu SK, Vadlani PV, et al. (2012). Statistical optimiza-tion of hydrolysis process for banana peels using cellulolytic andpectinolytic enzymes. Food Bioprod Process, 90, 257–65.
Oberoi HS, Vadlani PV, Nanjundaswamy A, et al. (2011b). Enhancedethanol production from Kinnow mandarin (Citrus reticulate) wastevia a statistically optimized simultaneous saccharification andfermentation process. Bioresour Technol, 102, 1593–601.
Obro J, Harholt J, Scheller HV, et al. (2004). Rhamnogalacturonan I inSolanum tuberosum tubers contains complex arabinogalactan struc-tures. Phytochem, 65, 1429–38.
Olano-Martin E, Gibson GR, Rastall RA, et al. (2002). Comparison ofthe in- vitro bifidogenic properties of pectins and pectic-oligosac-charides. J Appl Microbiol, 93, 505–11.
Olano-Martin E, Rimbach GH, Gibson GR, et al. (2003b). Pectin andpectic-oligosaccharides induce apoptosis in in vitro human colonicadenocarcinoma cells. Anticancer Res, 23, 341–6.
Olano-Martin E, Williams MR, Gibson GR, et al. (2003a). Pectins andpectic oligosaccharides inhibit Escherichia coli O157:H7 Shiga toxinas directed towards the human colonic cell line HT29. FEMSMicrobiol Lett, 218, 101–5.
Onumpai C, Kolida S, Bonnin E, et al. (2011). Microbial Utilization andSelectivity of pectin fractions with various structures. Appl EnvironMicrobiol, 55, 5747–54.
Panesar PS, Bali V, Kumari S, et al. (2014). Prebiotics. In: Brar SK,Dhillon GS, Soccol CR, eds. Biotransformation of waste biomass intohigh value biochemicals. New York: Springer, 237–59.
Parenicova L, Benen JAE, Kester HCM, et al. (2000). pgA and pgBencode two constitutively expressed endopolygalacturonases ofAspergillus niger. Biochem J, 345, 637–44.
Pedrolli DB, Biscaro D, Monteiro AC, et al. (2012). Pectin andpectinases: production, characterization and industrial application ofmicrobial pectinolytic enzymes. Biotechnol J, 3, 9–18.
Ralet MC, Bonnin E, Thibault JF, et al. (2001). Pectins. In: VandammeE, ed. Biopolymers. 6th ed. Weinheim: Wiley-VCH Verlag, 345–80.
Remoroza C, Buchholt HC, Gruppen H, et al. (2014). Descriptiveparameters for revealing substitution patterns of sugar beet pectinsusing pectinolytic enzymes. Carbohydr Polym, 101, 1205–15.
Renard CMGC, Crepeau M-J, Thibault J-F, et al. (1995a). Structure ofthe repeating units in the rhamnogalacturonic backbone of apple, beetand citrus pectins. Carbohydr Res, 275, 155–65.
Renard CMGC, Thbault JF, Mutter M, et al. (1995b). Some preliminaryresults on the action of rhamnogalacturonase on rhamnogalacturonanoligosaccharides from beet pulp. Int J Biol Macromol, 17, 333–36.
Roberfroid MB. (1996). Functional effects of food components on thegastrointestinal system. Nutr Rev, 54, S38–42.
Rodrı́guez G, Rodriguez R, Guillen R, et al. (2007). Effect of steamtreatment of Alperujo on the enzymatic saccharification and in vitrodigestibility. J Agric Food Chem, 55, 136–42.
Schemin MHC, fertonani HCR, Waszczynskyj N, et al. (2005).Extraction of pectin from apple pomace. Brazil Arch Biol Technol,48, 259–66.
Schols HA, Bakx EJ, Schipper D, et al. (1995). A xylogalacturonansubunit present in the modified hairy regions of apple pectin.Carbohydr Res, 279, 265–79.
12 N. Babbar et al. Crit Rev Biotechnol, Early Online: 1–13
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
Schols HA, Voragen AGJ. (2002). The chemical structure of pectins. In:Seymour GB, Knox JP, eds. Pectins and their manipulation. Oxford:Blackwell Publishing Ltd.; 1–30.
Shevchik VE, Hugouvieux CPN. (1997). Identification of a bacterialpectin acetyl esterase in Erwinia chysanthemi 3937. Mol Microbiol,24, 1285–301.
Sila DN, Buggenhout SV, Duvetter T, et al. (2009). Pectins in processedfruits and vegetables: part II – structure, function relationships. ComprRev Food Sci Food Saf, 8, 88–104.
Strasser GR, Amado R. (2001). Pectic substances from red beet(Beta vulgaris conditiva). Part I. Structural analysis of rhamnoga-lacturonan I using enzymic degradation and methylation analysis.Carbohydr Polym, 44, 63–70.
Sun RC, Hughes S. (1999). Fractional isolation and physiochemicalcharacterization of alkali-soluble polysaccharides from sugarbeetpulp. Carbohydr Polym, 54, 73–82.
Suzuki T, Yokotani KT, Tsubura H, et al. (2002). Plant growth promotingoligosaccharides produced from tomato waste. Bioresour Technol, 81,91–6.
Takano Y, Sato N, Mizuno M, et al. (2010), Abstract 59th AnnualMeeting of the Japanese Society Applied Glycoscience, Bp2-19,Shizuoka, Japan.
Thomassen LV, Meyer AS. (2010). Statistically designed optimization ofenzyme catalyzed starch removal from potato pulp. Enzyme MicrobiolTechnol, 46, 297–303.
Thomassen LV, Vigsnæs LK, Licht TR, et al. (2011). Maximal release ofhighly bifidogenic soluble dietary fibers from industrial potato pulp byminimal enzymatic treatment. Appl Microbiol Biotechnol, 90, 873–84.
Turquis T, Rinaudo M, Taravel FR, et al. (1999). Extraction of highlygelling pectic substances from sugar beet pulp and potato pulp:influence of extrinsic parameters on their gelling properties. FoodHydrocolloids, 13, 255–62.
Van Laere KMJ, Hartemink R, Bosveld M, et al. (2000). Fermentation ofplant cell wall derived polysaccharides and their correspondingoligosaccharides by intestinal bacteria. J Agric Food Chem, 48,1644–52.
Vigsnaes LK, Holck J, Meyer AS, et al. (2011). In Vitro fermentation ofSugar Beet arabino-oligosaccharides by fecal microbiota obtainedfrom patients with ulcerative colitis to selectively stimulate the growthof Bifidobacterium spp. and Lactobacillus spp. Appl EnvironMicrobiol, 77, 8336–44.
Vincken JP, Schols HA, Oomen RJFJ, et al. (2003). If homogalacturonanwere a side chain of rhamnogalacturonan I. Implications for cell wallarchitecture. Plant Physiol, 132, 1781–9.
Voragen AGJ, Coenen GJ, Verhoef RP, et al. (2009). Pectin, aversatile polysaccharide present in plant cell walls. Struct Chem, 20,263–75.
Vos AP, Haarman M, Van GJW, et al. (2007). Dietary supplementa-tion of neutral and acidic oligosaccharides enhances Th1-depend-ent vaccination responses in mice. Pediatr Allergy Immunol, 18,304–12.
Watt DK, Brasch DJ, Larsen DS, et al. (1999). Isolation, characterisa-tion, and NMR study of xyloglucan from enzymaticallydepectinised and non-depectinised apple pomace. Carbohydr Polym,39, 165–80.
Westphal Y, Kuhnel Stefan, Waard P, et al. (2010). LC/CE-MS tools forthe analysis of complex arabino-oligosaccharides. Carbohydr Res,345, 2239–51.
Willats WGT, McCartney L, Mackie W, et al. (2001). Pectin: cellbiology and prospects for functional analysis. Plant Mol Biol, 47,9–27.
Wong D. (2008). Enzymatic deconstruction of backbone structures of theramified regions in pectins. Protein J, 27, 30–42.
Yapo BM, Lerouge P, Thibault JF, et al. (2007). Pectins from citrus peelcell walls contain homogalacturonans homogenous with respect tomolar mass, rhamnogalacturonan I and rhamnogalacturonan II.Carbohydr Polym, 69, 426–35.
Yoon KY, Cha M, Shin SR, et al. (2005). Enzymatic production of asoluble fibre hydrolyzate from carrot pomace and its sugar compos-ition. Food Chem, 92, 151–7.
Zandleven J, Sorensen SO, Harholt J, et al. (2007). Xylogalacturonanexists in cell walls from various tissues of Arabidopsis thailiana.Phytochemistry, 68, 1219–26.
Zopf D, Roth S. (1996). Oligosaccharide anti-infective agents. Lancet,347, 1017–21.
Zykwinska A, Boiffard MH, Kontkanen H, et al. (2008). Extraction ofgreen labeled pectins and pectic oligosaccharides from plantbyproducts. J Agric Food Chem, 56, 8926–35.
Zykwinska A, Rondeau-Mouro C, Garnier C, et al. (2006).Alkaline extractability of pectic arabinan and galactan and theirmobility in sugar beet and potato cell walls. Carbohydr Polym, 65,510–20.
DOI: 10.3109/07388551.2014.996732 Pectic oligosaccharides from agricultural by-products 13
Cri
tical
Rev
iew
s in
Bio
tech
nolo
gy D
ownl
oade
d fr
om in
form
ahea
lthca
re.c
om b
y 81
.244
.40.
125
on 0
2/03
/15
For
pers
onal
use
onl
y.
Top Related