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Meat Science 98 (2014) 4757

Contents lists available at ScienceDirect

Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Review

Potential applications of plant based derivatives as fat replacers,


antioxidants and antimicrobials in fresh and processed meat products
Desugari Hygreeva , M.C. Pandey, K. Radhakrishna
Freeze Drying and Animal Products Technology Division, Defence Food Research Laboratory, Mysore, India

a r t i c l e

i n f o

Article history:
Received 25 April 2013
Received in revised form 15 April 2014
Accepted 23 April 2014
Available online 4 May 2014
Keywords:
Plant derivatives
Meat products
Natural antioxidants
Lipid oxidation
Vegetable oils
Natural antimicrobials and microbial spoilage

a b s t r a c t
Growing concern about diet and health has led to development of healthier food products. In general consumer
perception towards the intake of meat and meat products is unhealthy because it may increase the risk of
diseases like cardiovascular diseases, obesity and cancer, because of its high fat content (especially saturated
fat) and added synthetic antioxidants and antimicrobials. Addition of plant derivatives having antioxidant
components including vitamins A, C and E, minerals, polyphenols, avanoids and terpenoids in meat products
may decrease the risk of several degenerative diseases. To change consumer attitudes towards meat consumption, the meat industry is undergoing major transformations by addition of nonmeat ingredients as animal fat replacers, natural antioxidants and antimicrobials, preferably derived from plant sources.
2014 Elsevier Ltd. All rights reserved.

Contents
1.
2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Effects of plant based derivatives on lipid oxidation and shelf life extension of meat products
2.1.
Fruit and vegetable extracts as natural antioxidants . . . . . . . . . . . . . . . .
2.2.
Herbs and spice extracts as natural antioxidants . . . . . . . . . . . . . . . . .
3.
Role of plant derivatives in the development of low fat healthier meat products . . . . . .
3.1.
Vegetable oils and low fat meat products . . . . . . . . . . . . . . . . . . . .
3.2.
Plant bers and low fat meat products . . . . . . . . . . . . . . . . . . . . .
4.
Role of plant extracts as natural antimicrobials in meat products . . . . . . . . . . . . .
5.
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction
Changes in lifestyle and eating habits of human beings, has been
shown by researchers and health organizations (World Health Organization (WHO), Food And Agriculture Organization (FAO)) to be the
major cause of increases of diseases like, obesity, cancer, cardio vascular
failures, (Jimenez-Colmenero, Muniz, Alonso, & Collaborators, 2010;
Corresponding author at: Freeze Drying and Animal Products Technology Division,
Defence Food Research Laboratory, Mysore-570011, Karnataka, India. Tel.: + 91
9886813258; fax: +91 8212473468.
E-mail address: hayagreevafoodtech@gmail.com (D. Hygreeva).

http://dx.doi.org/10.1016/j.meatsci.2014.04.006
0309-1740/ 2014 Elsevier Ltd. All rights reserved.

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47
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WHO, 2003). Nowadays people are showing greater interest in foods


that contain bioactive or functional components which will give additional benets to their health status (Cofrades, Serrano, Ayo, Carballo,
& Jimenez-Colmenero, 2008). As Hippocrates said let food be thy medicine and medicine be thy food is now seen in the development of
healthier, functional food products. Food products are important and
suitable vehicles for the human beings to carry and deliver the essential
nutrients that may improve their wellbeing. Among foods, meat and
meat products occupy a prominent position in the human diet because
of their high quality protein content, essential amino acids and excellent
source of B-group vitamins, minerals and other nutrients, (Zhang, Xiao,
Samaraweera, Lee, & Ahn, 2010). Many consumers believe meat and

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D. Hygreeva et al. / Meat Science 98 (2014) 4757

meat product consumption is unhealthy, because of their high animal


fat, cholesterol, synthetic antioxidants and antimicrobials contents
which may be associated with the several degenerative diseases
(Serrano, Librelotto, Cofrades, Snchez-Muniz, & Jimnez-Colmenero,
2007). Food technologists and nutritionists have been making great
efforts to develop novel meat products with low fat and low sodium
contents containing natural antioxidants and antimicrobials and
enriched with dietary bre and -3 and -6 fatty acids (Fig. 1).
Development of healthy food products is possible in two ways one
is decreasing the undesired substances and other is by increasing the
levels of desired healthier components (Decker & Park, 2010). This
strategy could be employed for the development of healthier meat
products.
Presently researchers are showing great interest in the utilization of
plant based derivatives derived from nuts, fruits, vegetables, herbs and
spices for the development of modied and healthier meat products
with improved shelf life (Fig. 2). The present review aims to evaluate
the present scenario in meat research for the development of healthier
and shelf stable meat products by the successful utilization of plant
based materials/derivatives.

2. Effects of plant based derivatives on lipid oxidation and shelf life


extension of meat products
Among foods, meat is one of the most prone to bacterial spoilage and
oxidative deterioration under normal storage conditions (Fung, 2010).
Lipid oxidation is a chemical process that involves the development of
off odors and decreases the acceptability of meat and meat products
by deterioration of their color, texture and nutritive value (Kanner,
1994). Meat and meat products when subjected to processing (heat)
and storage undergo changes in their physical and chemical characteristics that leads to development of oxygenated free radicals which initiate the oxidation of polyunsaturated fatty acids while destruction of the

natural antioxidant systems. In general, development of shelf stable


meat products involves the use of synthetic polyphenolic antioxidants
such as butylated hydroxy anisole (BHA), butylated hydroxyl toluene
(BHT) and tertiary butyl hydroxy quinine (TBHQ) to delay lipid oxidation, by reacting with the free radicals and chelating metal ions such
as, copper and iron which act as catalysts of the oxidation process. However consumer concerns about the safety of synthetic antioxidants in
foods, led to the utilization of natural antioxidants in meat and meat
products as alternative antioxidants to preserve the food, with additional health benets. For instance consumption of plant extracts that are
rich in natural phenolic compounds (eg, grape seed extract, green tea
extract, black currant extract) are reported to decrease the risk of several degenerative diseases such as obesity, atherosclerosis and cancers
and extend the shelf life of meat and meat products by delaying oxidation and microbial spoilage (Bagchi et al., 2000; Jia, Kong, Liu, Diao, &
Xia, 2012).
Addition of natural antioxidants to meat and meat products is one of
the important strategies in development of healthier and novel meat
products. In this regard several studies utilizing herbs, spices, fruits
and vegetable extracts, and have shown that addition of these extracts
to raw and cooked meat products decreased lipid oxidation, improved
color stability and total antioxidant capacities which are important
characteristics for shelf stable meat products (Table 1). The major active
components/phytochemicals responsible for the antioxidant activity of
plant derivatives are polyphenols, avonoids, phenolic diterpenes
and tannins (Zhang et al., 2010). Table 1 summarises studies reporting
antioxidant and lipid oxidation inhibition activities of plant derivatives
in meat products.

2.1. Fruit and vegetable extracts as natural antioxidants


Fruits and vegetables are one of the richest sources of natural polyphenols. Plant polyphenols have strong antioxidant activity against

Fig. 1. Healthier meat products and their characteristics.

D. Hygreeva et al. / Meat Science 98 (2014) 4757

49

Fig. 2. Plant based derivatives and their major phytochemicals responsible for healthier lipid prole, antioxidant and antimicrobial activity in meat products.

free radicals developed during oxidation in living organisms as well as


in muscle foods. Therefore plants or their derivatives that are rich in
polyphenols such as grape seed extract, cocoa leaves, broccoli extract,
green tea extract have shown antioxidant activity in meat and meat
products (Zuo, Wang, & Zhan, 2002).
Grape seed extract has been reported to be one of the richest sources
of natural polyphenols, comprising avanols, phenolic acids, catechins,
proanthocyanidins and anthocyanins. Among these, catechins and
proanthocyanidins are the major groups representing about 77.6% of
total polyphenols (Silvan et al., 2013). The high amount of phenol
groups in grape seed extract explains their strong lipid oxidation inhibition and antimicrobial activity in raw and cooked muscle foods (Ahn,
Grun, & Mustapha, 2007; Brannan, 2008).
Mielnik, Olsen, Vogt, Adeline, and Skrede (2006) found that
during refrigerated storage (13 days) of vacuum packed cooked turkey
breast meat, addition of varying levels of grape seed extract (0.0, 0.4, 0.8,
1.6/kg) inhibited oxidative rancidity (up to 83.72%) and volatile compounds formation (up to 89.83%). The efciency of inhibition was
concentration dependent and grape seed extract showed maximum inhibitory effect at 1.6%/kg. Kulkarni, DeSantos, Kattamuri, Rossi, and
Brewer (2011) compared grape seed extract (100, 300, 500 ppm) with
ascorbic acid and propyl gallate (100 ppm of fat) in lean beef sausages
cooked (70 C) sliced and stored at 18 C for 4 months and concluded
that samples prepared with the grape seed extract (100,300 ppm) and

propyl gallate retained their freshness, had less rancid odour and had
lower thiobarbituric acid reactive substances (TBARS) values compared
to controls and ascorbic acid containing samples during the storage period. Moreover, it was demonstrated that, frankfurters prepared with addition of different concentrations (0, 0.5, 1, 2, 3, 4, 5%) of grape seed our,
had lower oxidation level and enhanced protein and total dietary ber
content with increasing levels of grape seed our (zvural & Vural,
2011).
In a study by Bastida et al. (2009) the addition of condensed tannins
of carob fruit extracts in non-puried (Liposterine-30 g/kg) and puried forms (Ex-Xenterol-30 g/kg) signicantly reduced TBARS numbers
and polar material content in cooked pork meat during six months of
chilled and frozen storage compared with -tocopherol (250 mg/kg).
The foremost quality and sensory attribute which inuences the
consumer acceptance of the meat and meat products is color (Jo, Jin, &
Ahn, 2000). The changes in color show the rate of oxidation of myoglobin, which is inuenced by lipid oxidation. Apart from lipid oxidation itself, the susceptibility of meat proteins to oxidative reactions during
heating and storage leads to deleterious changes in meat quality including water holding capacity, color and overall nutritional quality (loss of
essential amino acids) (Jongberg, Trngren, Gunvig, Skibsted, & Lund,
2012; Lund, Heinonen, Baron, & Estvez, 2011). Protein oxidation is a
complex phenomenon that involves a radical chain reaction (initiation,
termination and propagation), which causes oxidative damage to the

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D. Hygreeva et al. / Meat Science 98 (2014) 4757

Table 1
Antioxidant and lipid oxidation inhibition activity of plant based derivatives in meat products.
Plant derivative

Meat products and treatment dosage

Storage period and research outcome

Reference

Green tea extract


Sage essential oil

Dry fermented turkey sausage


Raw and cooked pork

Bozkurt (2006)
Fasseas et al. (2007)

Sage

Minced chicken breast

Decreased TBARS formation


Decreased TBARS values by 75%(raw) and
86%(cooked)
Controlled lipid oxidation

Kinnow rind powder, pomegranate rind


powder and pomegranate seed powder
Pomegranate fruit juice phenolics

Cooked goat meat patties

Rosemary extract

Cooked pork patties(200 ppm)

Grape seed extract

Cooked Ground beef (1%)

Ground cinnamon and cloves

Cooked meat of beef, pork and


mutton(250 mg/100gm)
Pork belly and pork loin
5% onion/garlic
Raw ground beef and patties(cooked
to an internal temperature 75 C)
1% concentration
Cooked pork patties
80 g/gm and 1000 g/gm

Garlic and onion powders


Oleoresin of rosemary

Bearberry extract

Crude cranberry extract

Chicken meat(dipping media)

Cooked pork

Lowered TBARS content up to 67%


12 days 4Cstorage
Lowered TBARS values 28 days 4 C storage
Lowered TBARS and hexanal counts
compared with control
Decreased TBARS values by 92%
9 days 4 C storage
Controlled TBARS formation
6 days 5 C storage
Reduced TBARS numbers
8 C for 28 days
Reduced TBARS numbers and hexanal
values signicantly compared to control
4oc for 9 days
Inhibited TBARS formation
1000 g/gm 9 fold reduced lipid oxidation
4 C for 4 days
51% inhibited TBARS formation
2 C for 9 days

Mariutti, Orlien, Bragagnolo,


and Skibsted (2008)
Devatkal, Narsaiah, and Borah (2010)
Vaithiyanathan, Naveena, Muthukumar,
Girish, & Kondaiah (2011)
Nissen, Byrne, Bertelsen, & Skibsted (2004)
Ahn et al. (2007)
Jayathilakan, Sharma, Radhakrishna,
and Bawa (2007)
Park, Yoo, and Chin (2008)
Ahn et al. (2007)

Carpenter, O'Grady, O'Callaghan, O'Brien,


and Kerry (2007)
Lee, Reed, and Richards (2006)

TBARS = Thiobarbituric acid reactive substances.

muscle proteins by the reactive oxygen species (ROS) formed during


lipid oxidation and transition metals such as iron and copper (Vuorela
et al., 2005). In this regard studies have reported that addition of fruit
derivatives rich in polyphenols such as white grape extract, strawberry,
hawthorn, blackberry and pomegranate fruit phenolics to meats
(cooked burger patties) may inhibit lipid and protein oxidation through
radical chain inhibition and thus prevent color deterioration in
the product (Ganho, Morcuende, & Estvez, 2010; Jongberg, Skov,
Trngren, Skibsted, & Lund, 2011)
Studies have compared the efciency of fruit extracts in inhibiting
protein and lipid oxidation and found that such derivatives are more
potent in controlling lipid than protein oxidation in muscle foods
(Jongberg et al., 2012). The reason may be due to the greater sensitivity
of muscle lipids to oxidation than proteins. The covalent binding of
phenolic compounds present in the fruit/plant extracts to proteins
may mask their antioxidant/inhibitory effects on protein oxidation
(Estvez, Kylli, Puolanne, Kivikari, & Heinonen, 2008; Jia et al., 2012;
Lund, Hviid, & Skibsted, 2007).
Jia et al. (2012) reported that during chilled storage (4 C/9 d) the
addition of different concentrations of condensed black current extract
(Ribes nigrum. L), 5, 10 or 20 g/kg to pork patties decreased TBARS
values by 74.9, 90.6 and 91.7% but protein oxidation to a lesser extent
(compared with TBARS) in a dose dependent manner compared with
control samples. Moreover addition of BCE extract stabilized the color
of the patties during the storage period.
Rodrguez-Carpena, Morcuende, and Estvez (2011) observed that
during chill storage of raw porcine patties for 15 days the addition of
peel and seed extracts from two avocado varieties Hass and Fuerte resulted in lower TBARS values, and signicantly reduced the color loss.
Moreover Hass avocado extract signicantly inhibited the formation of
protein carbonyls in the chilled patties. The addition of red grape pomace extract (0.06 g/100 g) to pork burgers resulted in color stability,
lipid oxidation inhibition and yielded best overall acceptability after
6 days storage at 4 C under aerobic conditions (Dolores, Auqui, Mart,
& Linares, 2011).
Tomato is widely cultivated all around the world. The presence high
amounts of lycopene in tomato, which is a natural colorant (red) and
antioxidant is a functional ingredient that can be used in food products.
The addition of 10% tomato paste (TP) during the manufacture of

mortadella improved the nutritional status (Lycopene), color stability


and decreased lipid oxidation (control 59.17mm MDA/kg, TP treated
3040 mm MDA/kg) with on negative effect on consumer overall acceptance during 2 months storage at 4 C (Domnech-Asensi et al.,
2013). Additionally in vacuum packed irradiated ready to eat turkey
breast rolls the addition of 1, 2 and 3% concentration of plum extract increased a* and b* values and decreased L* values because of its natural
color compounds. More than 2% plum extract controlled lipid oxidation
and the production of aldehydes in these rolls (Lee & Ahn, 2005).
Green vegetables are rich in many bioactive components including
chlorophylls, vitamins, carotenoids and polyphenols. The occurrence
of wide range of phytochemicals that have the capacity to quench singlet oxygen species led to the use of green vegetables and their extracts
as natural antioxidants in food products (Gardner, White, McPhail, &
Duthie, 2000). Kim, Cho, and Han (2013), Kim, Min, et al. (2013)
assessed ten edible plant extracts from the fresh leaves of crown
daisy, pumkin, chamnamul, fatsia, leek, bok choy, acanthopanax,
butterbur, soybean, and the ower heads of broccoli (0.1 and 0.5%) for
their antioxidant activity in fresh ground beef. They compared the antioxidant activity of the plant extracts with BHT (0.1 and 0.5%) and reported that the addition of edible plant extracts signicantly lowered
TBARS values compared with non-treated samples. Moreover samples
treated with 0.5% butterbur had the same lipid oxidation inhibition
activity as 0.5% BHT and suggested that these plant extracts can be
used as potential natural preservatives in meat products. Banerjee
et al. (2012) examined the antioxidant potential of broccoli extract in
goat meat nuggets and observed that addition of extract to the nuggets
signicantly decreased the TBARS and pH values of the product. Moreover they compared the extract with butylated hydroxyl toluene
(BHT) and reported that total phenolics in 5 mg of extract was higher
than 100 ppm of BHT and 2.25 mg and 3 mg was similar to 50 and
100 ppm of BHT in free radical scavenging activity. Incorporation of
1.5% NaCl and 2% hydrolysed whey protein isolate or soy protein isolate
signicantly decreased the concentration of conjugated dienes and
TBARS values in cooked pork patties stored at 4 C for 7 days (PeaRamos & Xiong, 2003). Finally the addition of brined onion extracts
increased cooking yield and decreased TBARS values of turkey breast
rolls during 7 days storage at refrigerated temperatures (Tang &
Cronin, 2007).

D. Hygreeva et al. / Meat Science 98 (2014) 4757

Waste materials from the food processing industries are now an important resource for bio active components. DeJong and Lanari (2009)
reported that the crude polyphenol extracts from the waste waters of
olive oil inhibited lipid oxidation (TBARS values) in precooked beef
(6383%) and pork (4766%). Hassan and Swet Fan (2005) compared
the antioxidant potential of a polyphenol extract from cocoa leaves with
a mixture of synthetic antioxidants BHA/BHT (1:1 ratio 200 mg/kg) in
mechanically deboned cooked chicken meat stored at 4 C by analyzing
their peroxide, TBARS and hexanal generation values and observed that
the antioxidant potential of the extract (200 and 400 mg/kg) was about
5080% of that of BHA/BHT. Brettonnet, Hewavitarana, DeJong, and
Lanari (2010) reported that crude polyphenol extracts of canola (15 or
100 mg gallic acid equivalents (GAE/kg meat) reduced TBARS values
in precooked beef (6692%), chicken (3670%) and pork (4375%)
when stored at 4 C for six days.
2.2. Herbs and spice extracts as natural antioxidants
Extracts of herbs and spices are used as antioxidants, antimicrobials,
anti-diabetics, anticarcinogens, avorings, beverages and repellents.
The increasing interest of meat industry in natural antioxidants and
antimicrobials led to extensive research on the utilization of spice
and herb extracts as lipid oxidation inhibitors. The role of herbs and
spice extracts, including rosemary, oregano, clove, thyme and citrus
fruits were have been studied for their antioxidant potential in
cooked, fermented and irradiated meat products (Rodrguez Vaquero,
Tomassini Serravalle, Manca de Nadra, & Strasser de Saad, 2010).
Enhanced shelf life of cooked ground pork stored at 4 C for 14 days
has been seen. Treatment with different kimchi extracts, baechu kimchi
(BK-0.1%), got kimchi (GK-0.1%), puichu kimchi (PK-0.1%), and white
kimchi (WK-0.1%) signicantly lowered TBARS, peroxide and hexanal
contents. Among these GK showed good antioxidant activity compared
with ascorbic acid (0.02%), BHT (0.02%) and other extracts (Lee et al.,
2011). Juntachotea, Berghofera, Siebenhandla, and Bauerb (2007)
reported that the addition of dried galangal powder (0.05, 0.10 and
0.15%) and its ethanoloic extract (0.17, 0.43 and 0.51%) to cooked
pork during storage at 51 C for 14 days signicantly reduced TBARS,
peroxide and conjugated diene values and also inhibited the formation
of hexanal (highest inhibition observed at a concentration 0.51%
of ethanolic extract). Reya, Hopiab, Kivikarib, and Kahkonenb (2005)
studied the antioxidant activity of cloudberry, willow herb and beetroot
extracts (100 and 500 mg/kg) in comparison with pure quercetin, rutin
and caffeic acid. Lipid oxidation and hexanal content in cooked pork
patties were evaluated and these extracts helped in lowering lipid oxidation and reduced the hexanal content of patties (Reya et al., 2005).
Choe et al. (2011) evaluated the antioxidant activity of lotus leaf
powder, 0.1% (LP1), 0.5% (LP2) and barley leaf 0.1% (BP1), 0.5% (BP2)
powder in cooked ground pork and reported that addition of LP2 or
BP2 signicantly decreased lipid oxidation and lowered peroxide and
conjugated diene values when compared with control samples containing BHT (0.01%) during refrigerated storage for 10 days. There were
no signicant changes observed in overall acceptability among the
treatment groups (LP/BP). Qi and Zhou (2013) found that addition of
epicarp extract of lotus seed at 6.25, 12.5, 25, 50 and 100 g mL1 concentrations to pork homogenates retarded TBARS and peroxide values
in Chinese Cantonese sausages. Moreover the cytotoxic and anti obesity
activity of the extract in in vitro in 3 T3-L1 preadipocyte cell models
depended on the dosage; epicarp extracts of lotus seed are potent antioxidant and anti obesity phytochemicals with no toxic effects.
Fasseas, Mountzouris, Tarantilis, Polissiou, and Zervas (2007)
showed that porcine and bovine ground meat treated with the essential
oils of oregano and sage (3%W/W) had increased oxidative stability and
the antioxidant capacity of the raw and cooked meat (85 C for 30 min)
was high during storage at 4 C for 12 days. They also suggested that
addition of antioxidants is much more important for cooked meat products than the raw products. De Oliveira et al. (2012) manufactured

51

mortadella-type sausages with different levels of sodium nitrate


(0, 100, 200 mg/kg) and winter savory essential oil (7.80, 15.60 and
31.25 l/g) and stored them at 25 C for 30 days and observed lower
TBARS values in the products containing essential oil alone and essential
oil with reduced amounts of sodium nitrate.
Interestingly, Sampaio, Saldanha, Soares, and Torres (2012) found
that the combination of sage, oregano and 5 and 10% honey received
greater acceptability and exhibited better antioxidant activity, reducing
the TBARS and hexanal values, of cooked chicken meat stored at 4 C for
96 hours. Castro, Mariutti, and Bragagnolo (2011) found that addition of
colorico in raw and grilled chicken patties delayed lipid oxidation
protected the vitamin E and bixin contents in chicken patties during
120 days storage at 18 C.
Lara, Gutierrez, Timn, and Andrs (2011) evaluated the antioxidant
activity of natural extracts from rosemary (Nutrox-30 mg/100gm)
and lemon balm (Melinox-30 mg/100g) in cooked pork meat patties
packed in modied atmosphere. They observed that natural extracts
signicantly reduced the TBARS values and hexanal contents in products during 3 days storage under illumination. Compared with BHT
(20 mg/100g) Nutrox showed better inhibition of lipid oxidation,
without any adverse effects on overall acceptability. Concentrations of
1500 and 2500 ppm of rosemary extract signicantly reduced the
TBARS numbers in refrigerated fresh pork sausages and 2500 ppm of
rosemary extract exhibited equal activity to BHA/BHT (200 ppm) in
controlling lipid oxidation in precooked-frozen sausage (Sebranek,
Sewalt, Robbins, & Houser, 2005).
Enrichment of meat products with, healthier lipid fractions such as
omega-3 and omega-6 poly unsaturated fatty acids will enhance the
quality. At the same time the stability of these fatty acids is low as
they are prone to faster degradation due to lipid oxidation. Hence
medicinal herbs and spices have been used to stabilize these functional
ingredients in meat products. Berasategi et al. (2011) formulated a
bolonga type sausages enriched with omega-3 polyunsaturated fatty
acids. The stability of the sausages were studied with the addition of
ethanolic extracts of Melissa ofcinalis and compared with the synthetic
antioxidant butylated hydroxy anisole (BHA). Sausages with BHA and
Melissa extract showed higher antioxidant capacity and had signicantly lower peroxide values (2.62 and 6.11 meqO2/kg) and thiobarbituric
acid (TBA) values (0.26 and 0.27 mg malondialdehyde/kg). Estevez,
Ramrez, Ventanas, and Cava (2007) reported that addition of sage
and rosemary essential oils to liver patties signicantly reduced the
losses of poly unsaturated fatty acids, lowered the total amount of
lipid derived volatiles and helped in retarding lipid oxidation when
compared with BHT during 0, 30, 60, 90 days of refrigerated storage.
In the meat sector, among all existing non thermal technologies,
irradiation is a safe and effective processing and decontamination technology. Although irradiation is recognized as an effective technology to
improve the microbial safety of meat and meat products, it can also be a
factor in initiating oxidation of lipids, leading to the formation of lipid
oxidation derivatives and cholesterol products (Nam, Du, Jo, & Ahn,
2001)
Trindade, Mancini-Filho, and Villavicencio (2010) proved that in irradiated beef burgers the addition of rosemary (400 mg/kg) and oregano
(400 mg/kg) extracts individually or in combination (200 mg rosemary
plus 200 mg oregano) and with either BHA/BHT (200 mg/kg) or their
blend (100 mg/kg BHA/BHT plus 200 mg/kg rosemary/oregano) decreased lipid oxidation (TBARS values 2.7 mg/kg control, treated
samples-below 2.0 mg/kg) in meat samples stored at 20 C
for 90 days. Further rosemary alone or in combination with either
BHA/BHT or oregano showed the highest inhibitory effect among all
the formulations.
Mohamed, Mansour, and Farag (2011) reported that addition of
herbal extracts of marjoram, rosemary and sage at concentration of
0.04 %(v/w) to ground beef prior to irradiation (2 and 4.5 kGy) signicantly lowered the TBARS values, off odour scores and increased colour
and acceptability scores. Subsequently other researchers proved that

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D. Hygreeva et al. / Meat Science 98 (2014) 4757

radiation processed lamb meat treated with mint leaf extract (0.1% and
0.5%) showed greater antioxidant activity and decreased lipid oxidation
(0.1% -18% and 0.5% -38%) during 4 weeks chilled storage compared
with non treated samples (Kanatt, Chander, & Sharma, 2007).
Jo, Son, Son, and Byun (2003) studied the effect of 70% ethanolic extracts of freeze dried green tea leaf (GTL), with and without irradiation
on the functional and sensory properties of raw and cooked pork patties.
They found that the addition of irradiated GTL extract (0.1%) inhibited
lipid oxidation, increased hunter color a* values and samples received
higher sensory scores compared with the non-irradiated samples containing the extract and the no extract added samples during storage
at 4 C for 15 days (Jo et al., 2003). Similarly Teets and Were (2008)
found that in minced chicken breast meat the addition of irradiated
almond skin powder (0.5%) signicantly reduced peroxide values
(066%), conjugated dienes (724%), TBARS (037%) and hexanal contents (471%) evaluated periodically for 12 days of refrigerated storage
and seven months of frozen storage, compared with the BHT (0.01%)
treated and no antioxidant untreated samples.
A number of studies have compared BHA and BHT with plant fruit,
vegetable and herb extracts for their antioxidant activity in various
meat products. Generally plant extracts exhibit better lipid oxidation inhibition in cooked, fermented and irradiation processed meat products
in comparison with synthetic antioxidants. Further studies are needed
on the functionality and stability of phytochemicals in the nal products
under different processing and storage conditions.
3. Role of plant derivatives in the development of low fat healthier
meat products
Fat is an essential component in meat and meat products responsible
for such quality characteristics as juiciness, texture, meaty avor,
cooking yield and characteristic aroma (Choi et al., 2013). The fat in
the meat and meat products in general has high amounts of saturated
fatty acids (SFA) and cholesterol. The recommendations of health
organizations to increase intake of healthier fats and their ratios in the

diet, led to the development of healthier meat and meat products by replacing animal fat with vegetable oils. The use of vegetable oils in low fat
meat products not only helps in improving the fatty acid proles
but also helps in increasing product stability in terms of lower lipid
oxidation, peroxide values, conjugated dienes and free fatty acids.
Many researchers have studied the quality characteristics of meat products prepared with partial or complete replacement of animal fat with
vegetable oils (Table 2).
3.1. Vegetable oils and low fat meat products
Considered as a potential strategy, replacing animal fat with vegetable oils, in modied and healthier meat products, may enrich the fatty
acid prole and result in low fat or low cholesterol containing products.
The total or partial replacement of pork fat with healthier oils,
formulated with olive, lin seed, sh oil and konjac gel (015%) in liver
patties resulted in lower levels of saturated (27.4% and 21.3%) and
mono unsaturated fatty acid (49.8% and 42.5%) and higher contents of
poly unsaturated fatty acids (Delgado-Pando, Cofrades, RodrguezSalas, & Jimnez-Colmenero, 2011). Addition of healthier oil, stabilized
in a konjac matrix increased -3 fatty acid content and reduced the
total fat content in frankfurters (Salcedo-Sandoval, Cofrades, RuizCapillas Prez, Solas, & Jimnez-Colmenero, 2013). Delgado-Pando,
Cofrades, Ruiz-Capillas, Triki, and Jimnez-Colmenero (2012) developed low fat liver patties by replacing pork back fat with healthier oils
(olive, linseed and sh oil) and konjac gel resulting in lower contents
of malonaldehyde (0.1130.343 mg/kg sample) during 85 days storage
at 2 C. Fresh pork sausages manufactured with partial replacement of
pork back fat (15%) with green tea catechins (GTC-200 mg/kg) and
green coffee antioxidant (GCA-200 mg/kg) added linseed oil (LO) or
sh oil (FO), increased linolenic acid from 1.34% to 8.91 % (LO) and
EPA (eicosapentaenoic acid) from 0.05% to 2.83% (FO). Addition of
GTC signicantly reduced the lipid oxidation in raw sausages containing
sh oil and lower lipid oxidation was observed in lin seed oil containing
samples stored in aerobic or modied atmosphere packages for 7 days

Table 2
Plant derivatives as animal fat replacers in healthier meat and meat products.
Plant derivative

Meat product

Changes in product

Reference

Inter-esteried palm, cotton seed


and olive oils
Inter-esteried palm, cotton seed
and olive oils

Frankfurters

Improved nutrient quality, due to changes in fatty acid


prole
Altered fatty acid composition
Oleic acid increased from 28.76 %(control)to
45.57%(palm oil) and 47.15(cotton seed oil)
Increased linoleic acid
Decreased saturated fatty acid and cholesterol content
Increased PUFA from 2.51%(control) to 46.43%(20%GPS)
Improved linoleic acid from 2.12(control) to
45.2(20%GPS)
Increased PUFA form 6.6%(control) to 26.6%(45%WNP)
Reduced cholesterol content about 41.3%

Vural and Javidipour (2002)

Frankfurters

Ground poppy seeds(GPS) 5, 10, 20% Beef burgers


concentration

Wall nut paste(WNP) 15,30,45%


Pre emulsied olive oil
60%
Lin seed oil
6.6%
Pre emulsied soy oil
15,20,25%

Pre emulsied ax seed oil and


canola oil

Olive oil emulsied alginate


PUFA = poly unsaturated fatty acids.
MUFA = mono unsaturated fatty acids.
SFA = saturated fatty acids.

Turkish sucuk
Sucuk
Dry fermented pork sausages

n-6/n-3 ratio decreased form 14.1(control)


1.72.1(modied)
Fermented pork meat sausage Cholesterol content decreased from 92.96 mg/100gm
(Chorizo De Pamplona)
(control) to87.71 mg/100gm (modied 25%)
Increased PUFA from 15.22 (control) to 23.96gm/100gm
(modied-25%)
Dutch type fermented sausages PUFA /SFA ratio increased from 0.30(control) to
0.420.48(canola oil)
0.490.71(ax seed oil)
n-6/n-3 ratio decreased from 11.20(control)
6.945.12(canola oil)
1.931.05(ax seed oil)
Sausages
Reduced nal fat content in the product
Increased MUFA content

Vural, Javidipour, and Ozbas (2004)

Gok, Akkaya, Obuz, and Bulut (2011)

Ercoskun and Demirci-Ercoskun (2010)


Kayaardi and Gok (2004)
Ansorena and Astiasaran (2004)
Muguerza, Ansorena, and Astiasaran (2003)

Pelser, Linssen, Legger, and Houben (2007)

Beriain, Gmez, Petri, Insausti, and Sarris (2011)

D. Hygreeva et al. / Meat Science 98 (2014) 4757

at 4 C (Valencia, O'Grady, Ansorena, Astiasarn, & Kerry, 2008).


Hsu and Yu (2002) suggested that coconut, palm, soybean, olive and
hydrogenated soybean oils were the best animal fat replacers for the
development of low fat kung-wans. Replacing beef fat (15, 30 and
50%) with hazel nut oil in sucuk (Turkish dry fermented sausage) significantly increased the MUFA and PUFA and MUFA + PUFA/SFA ratios
and lowered total cholesterol contents in the product (Yldz-Turp &
Serdaroglu, 2008).
Consumption of walnut in the diet has been shown to decrease
cardiovascular risks and the addition of walnut paste to meat products
may improve their quality characteristics. Serrano et al. (2005) studied
the addition of 20% walnut in restructured beef steaks and reported that
addition of walnut increased the amount of tocopherol, the polyunsaturated fatty acid ratio, and reduced the cholesterol content, as well as
improving the iron, calcium and manganese contents which may
present health benets to consumers. Serrano et al. (2007) developed
restructured beef steaks with different levels of fat, low (L 2% fat) medium (M 13% fat) and 20% added walnut (W12.65 fat) and subjected the
products to different cooking methods, conventional oven, microwave
oven, electric grill and pan frying. They reported that addition of walnut
helped in retention of moisture, fats, and minerals and conferred better
textural and cooking properties to the product compared with the low
and medium fat containing products. Ayo et al. (2007) developed frankfurters with 25% walnut and reported that addition of walnut improved
poly unsaturated fatty acid contents, amino acid proles and bio active
components like alpha, beta and gamma tocopherols, total dietary
ber, tannins and polyphenols compared with low fat (6%) and normal
fat sausages (16%). Cofrades et al. (2008) incorporated preheated
defatted walnut in meat products to replace meat protein and observed
that such addition enhanced their water and fat binding capacity during
thermal treatment and also improved the gelling ability of the myobrillar proteins. Development of low fat frankfurters with 20% canola
or 20% canola-olive oils (3:1) in combination with rice bran and walnut
extract improved the textural and nutritional properties of the products
when compared to 20% pork fat added samples (lvarez et al., 2012).
3.2. Plant bers and low fat meat products
Plants are important sources of dietary ber, and consumption of
dietary ber may reduce the risk of diseases such as gastrointestinal
disorders, coronary heart diseases, obesity, diabetes, hypertension and
many cancers (Anderson et al., 2009)
Plant bers are regarded as functional ingredients in meat products
in two ways, by decreasing the caloric content and by increasing the
complex carbohydrate content, which is low in meat products. Many
studies have successfully utilized plant dietary bers as partial fat
replacers, and reported that incorporation of dietary ber into meat
products may also enhance the binding properties, cooking yield and
textural characteristics of meat products, such as meat balls, patties,
sausages and bolognas (Borderas, Snchez-Alonso, & Prez-Mateos,
2005; Fernandez-Gins, Fernndez-Lpez, Sayas-Barber, Sendra, &
Prez-lvarez, 2004).
Fernandez-Gins et al. (2004) reported that addition of different
concentrations (0%, 2.5%, 5%, 7.5%and 10%) of lemon albedo (raw and
cooked) in bologna sausages increased the nutritional quality and
reduced nitrite levels. In another study, Choi, Choi, Han, Kim, Lee, Kim,
et al. (2010) replaced pork back fat with grape seed oil and rice bran
ber and developed reduced fat meat emulsion systems. They concluded that addition of grape seed oil and rice bran ber improved cooking
characteristics and successfully reduced the animal fat content in the
nal product. Sanchez-Zapata et al. (2011) studied the addition of
tiger nut ber (0%, 5%, 10%,15%) to pork burgers and evaluated the quality characteristics of burgers based on their physico-chemical, cooking
and sensory characteristics. They concluded that addition of tiger nut
ber in pork burgers signicantly improved the nutritional and cooking
characteristics of the product without affecting the sensory quality.

53

Other researchers proved that the addition of grape antioxidant dietary


ber signicantly increased the oxidative stability and radical scavenging activity in raw and cooked chicken hamburgers (Sayago-Ayerdi,
Brenes, & Goni, 2009). Sanchez-Zapata et al. (2011) formulated bologna
type sausages with up to 15% of date paste. Incorporation of date paste
enhanced the quality in terms of low fat, high ber content and
high emulsion stability without affecting the sensory attributes of the
product.
Huang, Shiau, Liu, Chu, and Hwang (2005) added four rice brans, of
different particle sizes to emulsied meat balls and reported that addition of less than 10 % rice bran did not affect the sensory quality but
the particle size of the bran profoundly affected the sensory and physicochemical characteristics of the product. Interestingly Garcia and
others(2002) fortied reduced fat dry fermented sausages with cereal
(1.5%) and fruit bres (3%) and observed that addition of 1.5% fruit
ber along with 10% of pork fat resulted in a better texture prole and
greater sensory acceptability. Yang, Choi, Jeon, Park, & Joo, 2007 developed low fat sausages by using hydrated oat meal or tofu at levels of
10%, 15%, and 25% as texture modifying agents and reported that addition of hydrated oat meal increased the water holding capacity and
cooking yield and produced a softer texture. Pietrasik and Janz (2010)
manufactured low fat bolognas with wheat our (as a standard binder)
or pea starch and bre as fat replacers which increased water holding
capacity and lowered cooking loss.
The addition of vegetable oils as animal fat replacers in meat products improves their fatty acid prole, in terms of increased polyunsaturated fatty acids, mono unsaturated fatty acids and natural antioxidants
(tochopherols, polyphenols) contents. Still there is need of research
pertaining to the stability of the PUFA, MUFA and SFA ratios in the products under different processing and storage conditions.
4. Role of plant extracts as natural antimicrobials in meat products
Meat is a good substrate for spoilage and pathogenic microorganisms because of its high moisture and nutrient contents (Enan,
Uyttendaele, El-Essawy, & Debevere, 1996; Zhang, Kong, Xiong, &
Sun, 2009). The major food borne microorganisms that are predominant and involved in the spoilage of meat and meat products are
shown in (Table 3). In foods antimicrobials are used for mainly for
two reasons: (1) to preserve the food for long time (control natural
spoilage process) and (2) to increase food safety (control growth of
pathogenic microorganisms).The term natural antimicrobials implies, antimicrobials derived from natural sources like plants, animals and microbes. The negative consumer perception towards
chemical antimicrobials/preservatives led to extensive search for
natural antimicrobials. In this context, essential oils and extracts of
medicinal herbs and spices have gained importance as natural preservatives with antimicrobial properties. There is huge potential for
usage of natural antimicrobials in food to control spoilage (Table 3).
The extracts and essential oils of herbs and spices are widely known
for their strong antioxidant, antimicrobial and antifungal activities in
foods. These properties of herb and spice extracts are due to the presence
of many bioactive components, including avanoids, terpenoids, vitamins, minerals, carotenoids and phytoestrogens (Rodrguez Vaquero
et al., 2010). Essential oils are the aromatic and volatile oily substances
consisting of mixtures of several active components derived from the
buds, owers, twigs, leaves, bark, wood, fruits and roots of the plant.
Some of the essential oils from oregano, rosemary, parsley, clove, lemongrass, sage and vanillin showed good antibacterial and antioxidant
properties in meat and meat products. In beef, pork, mutton, turkey,
and chicken meat products the addition of these herbs and spices and
their essential oils extracts inhibited the growth of several food borne
pathogens including Salmonella, Escherichia coli, Staphylococcus aureus,
Listeria monocytogenes, Shigella exneri and yeasts and molds (Table 3;
Hasapidou & Savvaidis, 2011), (Table 3). Moreover the use of natural
antimicrobials certied as generally recognized as safe (GRAS) has been

54

D. Hygreeva et al. / Meat Science 98 (2014) 4757

Table 3
Plant derivatives as natural antimicrobials in meat and meat products.
Plant derivative

Meat product

Antimicrobial activity and Effective against

Reference

Sage extract

Raw turkey meat balls

Reduced mesophyllic bacteria and coliform


counts
Reduced aerobic plate count
Inhibited Salmonella growth

Karpiska-Tymoszczyk, (2007)

Georgantelis, Ambrosiadis, Katikou, Blekas, and


Georgakis (2007)

Ground beef

Reduced microbial growth


Enterobacteriaceae
Pseudomonas species
Yeasts and molds
Lactic acid bacteria
Reduced coliform and Pseudomonas species

Emiroglu, Yemi, Cokun, and Candoan (2010)

Ground beef
Ham, beef and turkey

Suppressed growth of Listeria monocyotogenes


Suppressed growth of Listeria monocyotogenes

Qiu and Wu (2007)


Glass and Sindelar (2010)

Spanish dry fermented cured


sausages
Vacuum packed ground beef

Reduced mold contamination

Martin-Sanchez et al. (2011)

Controlled growth of Enterobacteriaceae

Michalczyk, Macura, Tesarowicz, and Bana


(2012)
Piskernik, Klancnik, Riedel, Brndsted, and
Mozina (2011)
Karabagias, Badeka, and Kontominas (2010)
Solomakos, Govaris, Koidis, and Botsoglou (2008)

Fresh garlic or garlic powder


Chicken sausage
Essential oils of Salvia Ofcianlis L. and Minced beef meat
Schinus Molle L.
Combination of Rosemary extract
Fresh pork sausages
Chitosan
Alpha tocopherol

Soy protein edible lms prepared with


incorporation of oregano and thyme
essential oil
Cranberry concentrate
Blend of lemon, cherry, vinegar
powder
Oregano essential oil
Essential oils of Coriandrum Sativum L
Hyssopus Ofcinalis L
Rosemary extract
Thyme and oregano essential oil
Thyme essential oil

Chicken meat and chicken meat juice Campylobacter jejuni


MAP packed fresh lamb meat
Minced beef meat

Reduced nal bacterial counts


Inhibited growth of E. coli O157:H7

widely accepted by consumers (Burt, 2004; De Oliveira et al., 2011).


However there is a lack of knowledge about the mechanisms, toxicological as well as the sensorial effects of naturally derived antimicrobials in
food (Gutierrez, Rodriguez, Barry-Ryan, & Bourke, 2008; Periago, Conesa,
Delgado, Fernndez, & Palop, 2006).
Viuda Mortas et al. (2009) observed that the shelf life of bologna sausages increased with the addition of orange dietary ber (1%) (ODB)
and oregano essential oil (0.02%) (OEO) under modied packaging conditions. This study showed that the sausages containing ODB and OEO
packed in vacuum had lower counts of aerobic and lactic acid bacteria.
Hsouna et al. (2011) evaluated the antimicrobial activity of Ceratonia
Siliqua pod essential oil in minced beef inoculated with the food borne
pathogen Listeria monocytogenes. They reported that the essential oil exhibited a strong inhibitory effect against the pathogen at 7 C. The combined addition of oregano essential oil (0.6%) and nisin (500 IU/g)
showed increased antimicrobial activity against Salmonella enteritidis
in minced sheep meat during storage at 4 C and 10 C for 12 days
(Govaris, Solomakos, Pexara, & Chatzopoulou, 2010).
Kim, Cho, et al. (2013) evaluated 10 leafy green vegetable
(LGV) extracts for their antioxidant and antimicrobial activity
against Escherichia coli, Salmonella enteric, Shigella exneri, Listeria
monocytogenes, Staphylococcus aureus and Bacillus subtilis. They added
the extracts in a concentration dependent manner to raw beef patties
and compared the effects to the synthetic antioxidant BHT. It was
found that addition of extracts and BHT signicantly decreased
the TBARS values, number of microorganisms and also improved the
colour stability. The authors concluded that among the LGV extracts
a Fatsia extract was the most effective antioxidant and antimicrobial.
Xi, Sullivan, Jackson, Zhou, and Sebranek (2011) found that addition
of cranberry powder at 1%, 2% and 3% resulted in 24 log CFU/gm less
growth of Listeria monocytogenes compared to the control. Other plant
extracts such as cherry powder, lime powder, and grape seed extract
showed measurable inhibition of Listeria monocytogenes when combined with cranberry powder. In another study addition of 3% cranberry
powder signicantly reduced Listeria monocytogenes growth by 5.3 log
CFU/gm in frankfurters (Xi, Sullivan, Jackson, Zhou, & Sebranek, 2012).
Hayrapetyan, Hazeleger, and Beumer (2012) used pomegrate (Punica
grantum) peel extract as a natural antimicrobial in chicken liver patties
stored at 4 C for 46 days and found signicant inhibition of Listeria

Sallama, Ishioroshi, and Samejima (2004)


Hayouni et al. (2008)

monocytogenes, by 4.1 log CFU/gm. In controls the microbial count


was 9.2 logs CFU/gm by the 18th day of storage.
The incorporation of spice and herb extracts inhibits major pathogenic
organisms such as salmonella Enteritidis, Listeria monocytogenes, and
Staphylococcus aureus in different meat products and adds natural
avoring to fermented meat products. Further investigation is needed
on the isolation of the phytochemicals responsible for the inhibitory activity of microorganisms and the impact of these extracts on sensory
attributes.
5. Conclusion
Plant based derivatives are widely available and are potential
sources for many bioactive components such as vitamins, minerals
and natural antioxidants such as tocopherols, polyphenols,
avanoids, tannins, terpenoids etc. The utilization of these derivatives as animal fat replacers, natural antioxidants and antimicrobials
in meat products may enhance product quality and can help the
meat industry to meet consumer demands for healthier meat products. Numerous studies have compared plant derivatives with synthetic antimicrobials and antioxidants and reported that they are
more potent and safer than synthetic compounds. Further research
has to be carried out on the extraction and isolation of the phytochemicals responsible for their antioxidant and antimicrobial activity and their potential applications in developing healthier, shelf
stable meat products.
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