Trends in Food Science & Technology 45 (2015) 37e49

Review

Alternatives to
nitrite in processed products has also increased with the novel concepts of
all-natural and clean-label (Jayasena & Jo, 2013).
Spoilage by microbes, autolytic enzymes and lipid
meat: Up to date oxidation can cause deterioration of meat and meat prod-
ucts, which has considerable economic and environmental
impact (Jayasena & Jo, 2013). Several thermal and non-
Amali U. Alahakoona, thermal meat preservation techniques, including refrigera-

Dinesh D. Jayasenab,
tion, freezing, drying, and smoking, are presently being
used in the meat processing industry (Sindelar &
Sisitha Ramachandrac and Milkowski, 2011).
Meat curing which includes the addition of salt, nitrite,
Cheorun Jod,* and sometimes nitrate to fresh meat cuts, enables preserva-
a
tive effect by removing moisture and reducing the water ac-
Department of Animal Science and Biotechnology, tivity of the meat (Parthasarathy & Bryan, 2012). In
Chungnam National University, Daejeon 305-764, addition to the preservative action, particularly against
Republic of Korea Clostridium botulinum, the curing process imparts several
b
Department of Animal Science, Uva Wellassa other distinctive properties that are common to all cured
University, Badulla 90000, Sri Lanka meat products which is attributable to the sodium nitrite
c
Department of Animal Science, University of present in the curing mixture (Sindelar & Milkowski,
Peradeniya, Peradeniya 20400, Sri Lanka 2011). These other properties include contribution to the
d formation of an unique color, texture, and flavor to cured
Department of Agricultural Biotechnology, Center for
Food and Bioconvergence, and Research Institute of meat products and protection of meat lipids from oxidation
Agriculture and Life Science, Seoul National (Sindelar & Milkowski, 2011). In the modern meat process-
University, Seoul 151-921, Republic of Korea ing industry, meat curing is a well-developed segment that
(Tel.: D82 28804804; fax: D82 28732271; e-mail: uses advanced techniques. In addition, nitrite plays a vital
[email protected]) role in normal human body functions (Sindelar &
Milkowski, 2012).
However, over the years, great concerns have been ex-
Nitrite has been used in different meat products mainly to pressed regarding the exposure of consumers to certain
maintain their microbial quality, flavor, and color and to pre- harmful products that may be formed in meat and meat
vent lipid oxidation. Since consumer demand for organic or products during and after curing. The foremost concern is
natural meat products has increased due to the concerns of that certain reaction products after curing may be carcino-
health risk of synthetic additives, the meat industry is currently genic to humans (Cassens, 1997a; Sen & Baddoo, 1997).
focusing on the development of nitrite alternatives. This paper This concern has led researchers to seek ways to reduce
reviews the potential alternatives to replace nitrite salts that are the risk of nitrosamine formation and alleviate potential hu-
used completely or partially in the manufacturing of meat man health concerns. One such way is the substitution of
products. nitrite with alternative ingredients having comparable char-
acteristics without causing any health hazards (Sindelar &
Milkowski, 2011). Over the past several decades, studies
Introduction have conducted to counter this difficult challenge; however,
The consumption of animal products including meat and until date, these attempts remained unsuccessful in identi-
meat products has increased globally with an increase in fying an effective single replacement material possessing
the household income (Nam, Jo, & Lee, 2010). In parallel, all the properties of nitrite (Sindelar & Milkowski, 2011).
the demand for safe and high quality meat and meat One possible approach to resolve this problem is the use
of hurdle technology in meat curing; in this approach,
* Corresponding author. low levels of sodium nitrite are combined with other
http://dx.doi.org/10.1016/j.tifs.2015.05.008
0924-2244/Ó 2015 Elsevier Ltd. All rights reserved.
38 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49

compounds and/or other processing technologies. It is of the denaturation of the protein moiety of the myoglobin
imperative that products treated with these secondary com- pigment (Parthasarathy & Bryan, 2012).
pounds or technologies be safe for human consumption. Although a minute amount of nitrite (2e14 ppm) is suf-
This review provides an overview of the published data ficient to develop a cured color in the meat, a higher
on the potential alternatives to completely or partially amount is necessary to avoid non-uniform curing and to
replace nitrite salt in meat and meat products. preserve the developed reddish-pink color throughout the
meat’s shelf-life (Sebranek & Bacus, 2007; Sindelar &
Nitrite in processed meat Milkowski, 2011). As the residual nitrite levels in cured
The precise discovery of meat curing may never be meat products gradually decline due to oxidation- and
known, but it is generally accepted to be associated with light-induced fading over the storage period (Cassens,
preservation methods using salt as early as 3000 B.C. 1997b), a residual nitrite level of 10e15 ppm is generally
(Sindelar & Milkowski, 2011). With the invention of refrig- recommended as a reservoir primarily for the regeneration
eration and food packaging technologies, the original role of cured meat color (Sindelar & Milkowski, 2011).
of curing technology of meat and meat products gradually
changed from that of preservative to that of development Cured flavor
to diverse convenient products (Pegg, 2004). The characteristic flavor of cured meat products can also
The main functions of nitrite in cured meat include the be attributed to the chemical reactions of nitrite and its
formation of the characteristic reddish-pink color and flavor associated reactions as described above. Sensory evaluation
associated with cured meats in addition to serving as an revealed that a low level of nitrite (50 ppm) was sufficient
effective antioxidant and antimicrobial agent alone or in to develop the unique flavor differences between cured and
combination with other ingredients (Pegg, 2004; Sindelar uncured meat. However, the principle mechanism and the
& Milkowski, 2011). Nitrate can be reduced to nitrite to compounds responsible for this unique flavor remain un-
perform the same function (Sindelar & Milkowski, 2011). known (Sindelar & Milkowski, 2011). Shahidi (1998) pro-
Therefore, naturally present or artificially supplemented ni- posed that this characteristic feature could be due to the
trate in brine solutions should be converted to nitrite by the nitrite-related suppression of oxidation products, which ma-
meat microflora or by the addition of bacteria possessing nipulates the development of rancid-flavor compounds.
nitrate reductase activity (Sebranek & Bacus, 2007). Sindelar and Milkowski (2011) suggested that cured meat
flavor could be the result of a combination of nitrite-
Cured color related flavors and aroma. Hydrocarbons, ketones, alcohols,
Nitrite e the true curing ingredient e is considered a phenols, esters, furans, pyrazines, aldehydes, and other ni-
multifunctional food additive that forms nitric oxide during trogen containing compounds, and increased carboxylic
the curing process. Formation of nitric oxide from the inter- acids, sulfur, and nitrite/nitrate containing compounds
mediates is facilitated by reductants such as ascorbate. It have been found in cured meat compared to uncured
has been recognized that nitrous acid (HNO2) is formed meat (Ramarathnam, Rubin, & Diosady, 1993). Alcohols
from nitrite under acidic conditions such as that in postmor- and phenols undergo nitrosation reactions and could impact
tem muscles (Pegg & Shahidi, 2000). According to Honikel volatile compounds as well. Increases in sulfur compounds
(2004), dinitrogen trioxide (N2O3) is formed from nitrous could be attributed to S-nitrosothiol formation and reduc-
acid and will subsequently form nitric oxide or will react tion to disulfide bonds during meat curing (Ramarathnam
with other substrates in meat. et al., 1993).
Nitric oxide will react with iron of both myoglobin
(Feþ2) and metmyoglobin (Feþ3) to form cured color Antioxidant effect
(Pegg & Shahidi, 2000). Comminuted meat quickly turns Another remarkable property of nitrite is its ability to
into brown color with the addition of nitrite due to metmyo- retard the development of rancidity during storage and
globin formation since nitrite acts as a strong heme pigment the subsequent warmed-over flavors developed upon heat-
oxidant and is, in turn, reduced to nitric oxide. Nitric oxide ing of meat and meat products (Parthasarathy & Bryan,
reacts with metmyoglobin and subsequent reduction reac- 2012; Pegg & Shahidi, 2000). The antioxidant activity of
tions convert the oxidized heme to reduced nitric oxide nitrite is attributed to the potential of nitric oxide to bind
myoglobin for typical cured color subjected to cooking to and stabilize heme iron of meat pigments during the
(Pegg & Shahidi, 2000). curing process. Oxygen and other reactive oxygen species
Nitric oxide reaction with myoglobin forms the nitrosyl- rapidly react with, and are sequestered by nitric oxide
myoglobin complex, which outline the basis for unique (Ford & Lorkovic, 2002). Nitric oxide, as a free radical,
cured meat color (Parthasarathy & Bryan, 2012). Nitrosyl- can also terminate lipid autooxidation (Pegg & Shahidi,
myoglobin is bright red in color (Parthasarathy & Bryan, 2000). In addition, it binds free irons and stabilizes heme
2012) and is an extremely unstable compound. During ther- iron (Bergamaschi & Pizza, 2011) which can reduce lipid
mal processing, it is converted to a stable, attractive oxidation by limiting prooxidant activity of iron. This
reddish-pink compound e nitrosohemochrome e because lowers the amount of free iron released during cooking
 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49 39

and chelates free radicals including lipid-derived alkyl, al- Nitrite can act as a nitrosating agent in the formation of
koxyl, and peroxyl radicals that accelerate lipid oxidation nitroso compounds (Cassens, 1995). N-nitroso compounds
in meat products (Parthasarathy & Bryan, 2012). Antioxi- belong to six fundamental categories: volatile N-nitrosa-
dant effect of nitrite has also been reported at levels as mine, non-volatile N-nitrosamine, N-nitrosamide, N-nitro-
low as 40 ppm (Al-Shuibi & Al-Abdullah, 2002). sated heterocyclic carboxylic products, N-nitrosated
glycosylarnines, and Amadori compounds (Hiramoto,
Kido, & Kikugawa, 1993). Several epidemiological studies
Antimicrobial effect
have demonstrated a potential relationship between nitrate,
Nitrite alone or in combination with other salts can
nitrite, and N-nitroso compounds and the risk of cancer
inhibit the growth of several aerobic and anaerobic micro-
(Alexander & Cushing, 2011). Certain nitroso compounds
organisms. Nitrite targets bacteria at multiple sites by in-
belong to a family of potent human carcinogens known
hibiting metabolic enzymes, limiting oxygen uptake, and
as N-nitrosodimethylamine; these nitrosamines are easily
breaking the proton gradient. In addition, nitric oxide
formed by interaction of a secondary amino compound
bound to iron, thus limits iron availability which is neces-
with nitrite under favorable conditions such as near acidic
sary for enzyme functionality and bacterial metabolism
pH and a product temperature of >130  C (Cassens,
and growth (Tompkin, 2005). Ironesulfur complexes and
1995). Although general health risks associated with nitrite
heme ion centers of enzymes are often the targets of nitrite
are known, Alexander and Cushing (2011) have reported
due to the high reactivity of iron and nitrite (Cui, Joannou,
that there is no supportive evidence to prove the relation-
Hughes, & Cammack, 1992).
ship between processed meat consumption and cancer
Moreover, nitrite is well-known to suppress the
risk. The exposure to only high overdoses of nitrite and ni-
outgrowth of C. botulinum spores in cured meat products
trate from different sources has been associated with
(Sindelar & Milkowski, 2011) and to completely control
increased incidence of health risks (Gangolli et al., 1994;
botulism. Nitrite has been reported to contribute to control-
Sanchez-Echaniz, Benito-Fernandez, & Mintegui-Raso,
ling the growth of several other pathogens such as Listeria
2001).
monocytogenes, Bacillus cereus, Staphylococcus aureus and
Meanwhile, studies conducted in the recent past have
Clostridium perfringens (Parthasarathy & Bryan, 2012;
suggested that nitrite is an important molecule for human
Pradhan et al., 2009).
health; it plays a prominent role in human physiology espe-
cially, in the endogenous production of nitrite in the human
Fate of nitrite in meat systems and health risk issues body. The major endogenous source of nitrate and nitrite in
Nitrite can react with or binds to several constituents mammals is the L-arginineenitric oxide pathway that is
within the meat systems as it is an extremely reactive com- active in numerous cell types throughout the body
pound. Its reactivity is increased by the heat applied during (Moncada & Higgs, 1993). Consequently, nitrite and nitrate
the thermal processing of cured meat products (Cassens, are produced in the blood and tissues by rapid oxidation of
1997b). In particular, the nitrite ion at pH < 7 is extremely nitric oxide. The reaction of nitric oxide with oxyhemo-
reactive; it can interact with various constituents of the globin in the blood mainly results nitrate and methemo-
meat such as amines, amino acids, sulphurhydryl, phenolic globin (Moncada & Higgs, 1993).
compounds, myoglobin, and reductants such as ascorbic Recent studies report that nitric oxide is involved in con-
acid (Toth, 1983). trolling blood flow in cardiac muscle and potentially other
The added nitrite in meat products could be completely tissues. Moreover, nitrite has a major role in mitochondrial
recovered as nitrate, nitrosylmyoglobin, gaseous nitrogen respiration and activation of the alpha form of the estrogen
compounds, and residual nitrite (Varnam & Sutherland, receptor, and applies an antiapoptotic effect to avoid cell
1995). Due to the combination of nitrite with meat pig- death (Bryan & Ignarro, 2010). In addition, the normal pro-
ments and other compounds, the detectable amount de- duction of nitric oxide and nitrite may prevent various types
clines rapidly during storage. Therefore, the residual of cardiovascular diseases, including hypertension, athero-
amount of nitrite is considerably lower compared to the sclerosis, and stroke (Sindelar & Milkowski, 2012). Oral
amount of the ingoing/added nitrite level (Cassens, 1996). microflora including Veillonella spp., S. aureus, Staphylo-
In addition, it has been reported that only 10e20% of the coccus epidermidis, Nocardia spp., and Corynebacterium
added nitrite could be analytically detected in cured meat spp. play a major role in nitrite-producing in human saliva.
immediately after processing (Cassens, 1997a). Sebranek This nitrite producing activity of aforementioned microor-
et al. (1973) reported the following fate of nitrite in cured ganisms is occurred with the contribution of combination
meat as the percentage of nitrite added: losses with protein of reducing substances in salivary secretions, reducing bac-
20e30%, with myoglobin 5e15%, as nitrate 1e10%, as ni- terial metabolites, mammalian nitrate reductase in the
trite 5e20%, as a gas 1e5%, with sulphydryl groups papilla linguae, and nitrate reductase enzymes of the micro-
5e15%, and with lipid 1e5%. These results indicate that organisms colonizing the tongue (Li et al., 1997). Since
the largest portion of the reacted or bound nitrite is associ- most of the ingested nitrite is formed in saliva, swallowing
ated with the protein component of the meat. saliva along with the food may result in the formation of
40 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49

nitroso compounds (Sindelar & Milkowski, 2011). There- retaining the properties of typical cured meat products
fore, processed meats are not the primary source of nitrate (Sebranek & Bacus, 2007). Celery powder was originally
or nitrite. In addition, vegetables, beer, and cereals can also available in its nitrate form; however, subsequently, pre-
vital sources of nitrate, nitrite and N-nitroso compounds converted celery powder was developed by some proces-
(Sindelar & Milkowski, 2011). sors, in which nitrate was converted to nitrite since the in-
Nitrite is difficult to replace as a preservative because it cubation step increased the processing time (Sebranek &
can serve multiple functions simultaneously. Although Bacus, 2007). It is considered that commonly used pre-
some studies have revealed that nitrite is not positively converted celery powder contains 10,000e15,000 ppm so-
related to health hazards in humans, a reduction or elimina- dium nitrite (Sindelar, Terns, Meyn, & Boles, 2010). How-
tion of nitrite usage is a key issue for the meat industry. ever, the addition of celery powder to processed meat is
Therefore, several studies are ongoing to examine the anti- generally limited to 0.2e0.4% of the formulation weight
microbial and sensorial effects of various alternative com- because at levels higher than this, off flavors may develop
pounds and/or technologies that can be used as nitrite (Sindelar et al., 2007). Since celery powder contains a sig-
substitutes. Therefore, organic or uncured meat production nificant amount of naturally occurring nitrate it will not be
currently plays a major role in the meat industry in order to the best alternative source of nitrite for meat without using
avoid direct usage of direct nitrite/nitrate. In this case, ni- in combination with nitrate reducing bacterial cultures to
trite is introduced indirectly through other ingredients produce a standard cured meat product. However, celery
into uncured meat products to achieve the quality, shelf- powder has only a very little amount of pigments and a
life, and safety improvements expected by modern-day mild taste that does not detract the flavor of meat.
consumers. Recently, spray-dried Swiss chard powder was used as a
natural source of nitrate. This product is similar to celery
Potential nitrite alternatives in processed meat powder and contains 3.0e3.5% nitrate and as for celery
The challenge for the meat industry is to search for stra- powder, this product should also be used at a concentration
tegies to reduce supplemented and residual nitrite in cured of 0.15e0.3% (Sebranek, Jackson-Davis, Myers, & Lavieri,
meat in order to minimize the nitrite intake. There is a 2012). High concentrations may negatively affect the sen-
considerable interest toward the development of alterna- sory attributes. The main advantage of Swiss chard powder
tives from natural sources and other preservation tech- is that it does not contain allergens (Sebranek et al., 2012).
niques that are considered to be comparatively healthier. In addition, Gabaza, Claeys, Smet, and Raes (2013) showed
This interest is further accelerated by the pressure gener- that fresh and dried spinach can be used as a source of ni-
ated from consumer demand for salt- and nitrite-reduced trate and that Staphylococcus carnosus can convert nitrate
meat products. to nitrite. Sebranek and Bacus (2007) reported that the ni-
The residual nitrite concentration in most of uncured trate level of spinach juice is approximately 3227 ppm.
products is generally lower than that in conventionally The residual nitrite content of fermented spinach-treated
cured products (Sebranek & Bacus, 2007; Sindelar, pork samples (50 g/L) was lower than that of nitrite-
Cordray, Sebranek, Love, & Ahn, 2007). Although it is treated samples (Gabaza et al., 2013).
difficult to replace nitrite by a single antimicrobial agent Phenolic compounds, organic acids, and flavonoids are
owing to its broad-spectrum activity (Pegg & Shahidi, the key antimicrobial and antioxidant compounds in most
2000), a combination of nitrite and different antimicrobial plant extracts. These compounds can damage the cell mem-
agents may be effective. However, any improvement mea- brane, which may lead to the leakage of cellular compo-
sures with regards to consumption safety should be under- nents, thereby inactivating or destroying microorganisms
taken without altering the unique characteristics of the (Oussalah, Caillet, Saucier, & Lacroix, 2006). The antioxi-
natural and organic processed meat products. dant property of these compounds can be attributed to their
characteristic to function as donors in the free radical chain
Plant-based alternatives reaction of lipid oxidation (O’Grady, Maher, Troy,
Considerable amount of nitrates are present in some veg- Moloney, & Kerry, 2006). The antioxidant and antimicro-
etables, which can be used as sources of nitrite. Vegetables bial properties of cranberry may be attributable to its
such as celery, spinach, radish, and lettuce have been re- organic acid content (citric acid, quinic acid, and malic
ported to contain more than 2500 mg nitrate/kg acid), and to the presence of anthocyanins, flavonol glyco-
(Santamaria, 2006). Celery juice and celery powder are sides, and proanthocyanidins (Chen, Zuo, & Deng, 2001;
frequently used as natural nitrate sources because they do Lee, Reed, & Richards, 2006). In addition, the residues
not impart any off-flavors owing to their high compatibility of tomato processing industries, including seeds and peels,
with processed meat products (Sebranek & Bacus, 2007). contain highly biologically active compounds such as ca-
Celery powder contains approximately 3% nitrate rotenoids (e.g., lycopene, b-carotene, phytoene, phyto-
(Sindelar et al., 2007) and is used by several meat proces- fluene, and lutein; Choksi & Joshi, 2007). Moreover,
sors along with a bacterial starter culture that reduces ni- carotenoids in tomato are among the most important groups
trate to nitrite during the manufacturing process while of natural pigments used as food colorants (Francis,
 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49 41

Barringer, & Whitemoyer, 2000). Both cranberry and to- reactive substances (TBARS) and improvements in sensory
mato extracts showed pH reductions that increase the qualities, including color and odor (Calvo, Garcia, &
amount of nitrite involved in the curing reactions when Selgas, 2008; Candogan, 2002; Sanchez-Escalante, Torres-
added together with nitrite and thus reduce the residual ni- cano, Djenane, Beltran, & Roncales, 2003; Yilmaz, Simsek,
trite concentration. Hence, the decreased pH observed in & Isiki, 2002). Therefore, it is obviously appropriate to use
these studies due to cranberry and tomato extracts may tomato in combination with nitrite in meat products to
have accelerated the nitric oxide production that led to avoid quality defects and to obtain maximum benefits.
the depletion of residual nitrite (Pegg & Shahidi, 2000; The antioxidative components in garlic are S-alkenyl
Xi, Sullivan, Jackson, Zhou, & Sebranek, 2011). cysteine sulfoxide and other sulfur components such as di-
Cranberry powder is a source of natural antimicrobial allyl disulphide and diallyl trisulphide (Sasse, Colindres, &
agents, particularly effective against L. monocytogenes Brewer, 2009). Antibotulinal properties of the majority of
growth in natural and organic processed meats (Qiu & spice extracts can be attributed to their constituents such
Wu, 2007). Although lemon and lime powders, and grape as eugenol, isoeugenol, D-borneol, citronellol, menthol,
seed extract are less effective against L. monocytogenes, cinnamic acid aldehyde, and rosemarin acid (Ueda,
they have the potential to control this organism in cured Yamashita, & Kuwabara, 1982). Moreover, the application
cooked meat when combined with cranberry powder (Xi of spices such as rosemary, thyme, sage, and garlic can
et al., 2011). These authors further reported that nitrite reduce the content of heterocyclic aromatic amines, thereby
(150 ppm initial nitrite) along with cranberry powder at reducing the formations of carcinogens in cooked cured
1, 2, and 3% concentration reduced the growth of L. mono- meat (Murkovic, Steinberger, & Pfannhauser, 1998). The
cytogenes by 2e4 log CFU/g as compared with only nitrite. active constituents in sage and rosemary are rosmanol,
However, the disadvantage regarding cranberry products is rosemadial, carnosol, carnosic acid, and epirosmanol
that it is slightly acidic in nature as they contain organic (Murkovic et al., 1998).
acids, which may eventually limit the amount of cranberry Cui, Gabriel, and Nakano (2010) used combinations of
product to avoid quality defects (Xi et al., 2011). Therefore, sodium nitrite and spice extracts from sage, clove, and
selection of the optimum concentration of this product for nutmeg and found them to successfully inhibit the growth
supplementation to processed meat is a crucial factor. of C. botulinum (sage) or inactivate (clove and nutmeg)
Deda, Bloukas, and Fista (2007) examined the quality the organism. The combined antibotulinal efficacy of
parameters of frankfurters produced with different levels nutmeg, sage, and clove extracts observed in this meat
of sodium nitrite and tomato paste. Frankfurters with low model system can be useful in the development of minimally
levels of sodium nitrite (50 and 100 ppm) and 12% tomato processed meat products, particularly those with low levels
paste showed the highest redness, whereas frankfurters with of sodium nitrite (approximately 10 ppm; Cui et al.,
12% tomato paste alone showed the lowest levels of resid- 2010). Ismaiel and Pierson (1990) noted diverse antibotuli-
ual nitrite. Therefore, the amount of nitrite added to frank- nal activities of sodium nitrite (50e100 ppm) and oregano
furters can be reduced from 150 to 100 ppm when essential oil (400 ppm) in ground pork. Furthermore,
combined with 12% tomato paste without any negative ef- Nevas, Koronen, Lindstrom, Turkki, and Korkeala (2004)
fect on the quality of the final product. In addition, Eyiler examined the antibacterial properties of essential oils
and Oztan (2011) stated that tomato powder retarded the derived from several spices against 12 bacterial strains
oxidation reaction and improved the consumer accept- including Escherichia coli, L. monocytogenes, Salmonella
ability in case of frankfurters. Furthermore, these authors Typhimurium, C. botulinum, C. perfringens etc. The authors
observed that increase in the amount of tomato powder re- found that oregano, savory, and thyme essential oils showed
sulted in increased redness values in the final product, the broadest range of antibacterial activity by inhibiting the
which is in agreement with the results of Deda et al. growth of all tested organisms. However, C. botulinum and
(2007). In addition, tomato powder has been shown to C. perfringens were the most sensitive among all organisms.
reduce the residual nitrite level in frankfurters as well as Since spice extracts could not provide all the functions that
to act as a natural colorant (Eyiler & Oztan, 2011). nitrite alone could do, it can be suggested to use spice ex-
Hayes, Canonico, and Allen (2013) stated that tomato tracts in combination with an appropriate amount of nitrite.
pomace powder, when incorporated at a concentration of Balentine, Crandall, O’Bryan, Duong, and Pohlman
1.5%, did not have any detrimental effects on the physico- (2006) demonstrated that processed meat treated with rose-
chemical properties of pork luncheon roll. The pork mary at a concentration of 3000 ppm could maintain the red
luncheon roll formulated with 50 ppm nitrite and 1.5% to- color for longer period and showed lower TBARS value.
mato pomace powder had similar or enhanced sensory attri- Doolaege et al. (2012) investigated the effects of different
butes and no negative effects on the texture, sensory doses of rosemary extracts (0, 250, 500, and 750 ppm) com-
qualities or the microbial stability as compared to those bined with low sodium nitrite levels (40, 80, and 120 ppm).
formulated with 100 ppm nitrite alone. Several studies The addition of rosemary extract positively retarded lipid
that tested tomato-based ingredients in meat products re- oxidation in liver pate. Furthermore, it was found that the
ported lower contents of nitrite and thiobarbituric acid concentration of sodium nitrite added to liver pate could
42 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49

be reduced from 120 to 80 ppm when rosemary extract was

Hernandez-Hernandez, Ponce-Alquicira,
added at all three concentrations, without any negative ef-

Jaramillo-Flores, and Legarreta (2009)

Apostolidis, Kwon, and Shetty (2008)

fect on lipid oxidation, antioxidant level, and color stability.

Ahn, Grun, and Mustapha (2007)

Bisha,Weinsetel, Brehm-Stecher,
Incorporation of citrus co-products in meat products is
another recent trend adopted for reducing the residual ni-

Zarringhalami, Sahari, and

trite concentration. The extracts of citrus co-products are

Liu, Wu, and Tan (2010)

Hamidi-Esfehani (2009)
rich in dietary fibers, antioxidant fibers, and bioactive com-

& Mendonca (2010)

pounds such as organic acid and polyphenols which can be

Tang et al. (2006)

Cui et al. (2010)

Mustafa (2013)
used as functional ingredients in meat products (Perez-
Alvarez, 2008).

References
Fernandez-Gines, Fernandez-Lopez, Sayas-Barbera,
Sendra, and Perez-Alvarez (2003) investigated the effects
of different concentrations of orange dietary fiber (0.5, 1,
1.5, and 2%) on the residual nitrite levels in a bologna-

No difference with 100 ppm nitrite added, color stability

Synergistic antibotulinal activity, reducing sodium nitrite
Reduced lipid oxidation and stabilized the meat color
type cooked sausage. The maximum reduction (69.57%)

Higher antioxidant activity and prevention of color

in the residual nitrite level was obtained with 2% orange di-

from 6e8 ppme2 ppm with 0.05% Coptis extract

C. perfringenes, control of C. botulinum growth

etary fiber in combination with 0.02% oregano essential oil
(Garcia-Martinez, 2009). The incorporation of orange die-

Improved lipid stability and color stability

tary fiber into dry-cured meat products resulted in reduced

Impact on growth of L. monocytogenes

Impact growth of L. monocytogenes,

residual nitrite levels as compared with that in the control

Impact growth of L. monocytogenes

Higher redness value, no growth of
and a higher redness value at levels >5 g/kg (Fernandez-
Lopez et al., 2007).
Several researchers studied the use of lemon albedo (raw
or cooked, dehydrated raw or dehydrated cooked) in
cooked and dry cured meat products for reducing the levels
of residual nitrite. Reduction in residual nitrite levels due to
the bioactive constituents of raw and cooked lemon albedo deterioration
(Fernandez-Gines, Fernandez-Lopez, Sayas-Barbera, Sen-
Effects

dra, & Perez-Alvarez, 2004). Aleson-Carbonell,

Table 1. Studies on potential usage of plant based alternatives for nitrites in meat products.

Fernandez-Lopez, Sendra, Sayas-Barbera, and Perez-

Alvarez (2004) investigated the influence of various con-
Cooked ground beef

Low-nitrite Chinese
centrations (0, 25, 50, 75, and 100 g/kg) of raw and cooked
Ground beef meat

Raw pork batters

Aqueous media

lemon albedo on the residual nitrite levels in dry-cured sau-

product/media
Type of meat

Cooked beef
Broth media
Beef patties

sages and found that raw albedo was more effective in

sausages
reducing the residual nitrite content and delaying lipid
Sausage
oxidation at all tested concentrations. Samples treated
with 50 g/kg dehydrated raw albedo and 75 g/kg dehy-
drated cooked albedo showed sensory properties similar
Oregano and cranberry (50:50)

Anka rice 0.5% 25 ppm nitrite

0.31, and 0.16% (v/v) in broth

at 750 ppm with 2% sodium

to those of the control. However, it is important to select

with 0.05% Coptis extract

60% in sausage and 0.08,

the best concentration since higher concentrations may

Sodium nitrite 6e8 ppm

exert a negative effect on sensory attributes. Table 1 pre-

Concentrations used

1% each ingredient

sents other potential plant-based alternatives for nitrite

0.00015e0.125%
0.02% of each

that can be used effectively in meat and meat products.

200 mg/kg

Organic acids
lactate
1e2%

The use of ions of organic acids such as lactate, acetate,

sorbate, and benzoate has been part of the food industry for
several years and has many different applications in wide
rhizome with sodium nitrite
Tea catechin with modified

Aqueous extract of Coptis

Annatto (Bixa orellana L.)

range of foods. Sodium and potassium lactate are widely

Oregano and cranberry,
atmospheric packaging
Potential alternatives

pine bark extract and

Anka rice with nitrite

incorporated in both fresh and cured meats (Brewer,

with sodium lactate
Grape seed extracts

Grape seed extract,

oleoresin rosemary

Rostogi, Argoudelis, & Sprouls, 1995; Kim et al., 2006).

Green tea extract

oregano extract

Presently, lactate is the most popular organic acid used

Rosemary and

as an antimicrobial agent in meat system since it is also

powder

known to enhance meat flavor owing to the salty taste

(Doores, 2005). Lactate has also been shown to improve co-
lor stability of fresh meat and to function as an antioxidant
 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49 43

(Brewer et al., 1995; Shelef, 1994). The addition of lactate effect was not due to lowering the water activity of the
may improve color stability by replenishing the reduced broth system used. Jones and Betts (2009) demonstrated
form of nicotinamide adenine dinucleotide (NADH) when that addition of 2% potassium lactate had an inhibitory ac-
lactate is converted to pyruvate by lactate dehydrogenase, tion on non-proteolytic C. botulinum in broth studies where
thereby increasing the metmyoglobin reducing activity. In 2% salt was present, the pH was 5.5 and the broths were
addition, deoxymyoglobin can convert nitrite to nitric ox- stored at 30  C.
ide; the generation of excess deoxymyoglobin in turn re- Furthermore, the use of benzoates as antibacterial com-
sults in the production of more nitric oxide and reduction pounds has received only a little attention compared to
in the residual nitrite level (Kim et al., 2006). other weak acid preservatives such as sorbates and lactates.
Ions of organic acids such as lactate, sorbate, and citrate Islam, Chen, Doyle, and Chinnan (2002) have shown that a
can exert antimicrobial effect specifically by changing wa- solution containing benzoate at a concentration of 25% (w/
ter activity, migrating through the cell membrane, lowering v) inhibited the growth of L. monocytogenes on the surface
the intracellular pH, and affecting cellular metabolism via of frankfurters. In addition, Jones and Betts (2009) demon-
inhibition of adenosine triphosphate (ATP) generation strated that 2000 ppm sodium benzoate had an inhibitory
(Maas, Glass, & Doyle, 1989). Sodium, potassium, and cal- action on non-proteolytic C. botulinum in broth studies
cium lactates are similar in their effectiveness in inhibitory where no salt was present.
activity against aerobic and anaerobic microorganisms in Moreover, studies conducted on bacon using potassium
meat (Shelef, 1994). Maas et al. (1989) investigated sorbate with low levels of nitrite have shown some success,
comminuted raw turkey containing 0, 2.0, 2.5, 3.0 or producing products of acceptable color and taste (Gray &
3.5% sodium lactate against a 10-strain mixture of C. bot- Pearson, 1984). However, complete replacement of nitrite
ulinum spores from proteolytic type A and B and showed with sodium sorbate is not possible since samples which
that sodium lactate exhibited an antibotulinal effect. contain sorbate solely being significantly unacceptable
Meng and Genigeorgis (1994) also examined the effect of due to increasing rancidity (Al-Shuibi & Al-Abdullah,
sodium lactate on toxigenesis caused by proteolytic and 2002). A previous study has shown allergic reactions to sor-
nonproteolytic C. botulinum spores inoculated in processed bate used as a nitrite alternative in meat, which caused
‘sous-vide’-type beef and chicken breast. Their results many to disregard its use (Gray & Pearson, 1984). Sorbates
showed that sodium lactate delayed toxin production in are not currently permitted as additives in any organic prod-
beef and chicken at >2.4 and > 1.8%, respectively. ucts and their permitted uses in non-organic meat products
Furthermore, Choi and Chin (2003) stated that sodium are very restricted. They are permitted in pate and in jelly
lactate influenced the growth of L. monocytogenes delaying coatings of cooked, cured or dried meat products in combi-
their lag phase by 2 wk, in addition affecting the growth of nation with p-hydroxybenzoates (Al-Shuibi & Al-
C. botulinum. Schlyter, Glass, Loeffelholz, Degnan, and Abdullah, 2002).
Luchansky (1993) demonstrated antilisterial effects of so- Lactates tend to be added to foods for their taste, buffering
dium diacetate (0.1, 0.3 and 0.5%) alone or in combination ability and humectant properties (Davidson, Sofos, &
with sodium nitrite (30 ppm), sodium lactate (2.5%) or ped- Branen, 2005). Lactic acid is currently permitted as an addi-
iocin (5000 AU/mL) in slurries prepared from ready-to-eat tive in the production of organic foodstuffs of either plant or
turkey breast meat. The increased antilisterial activity was animal origin, with no specific upper limit of usage set.
due to the synergistic effect of the combined treatments.
In addition, inhibition of the germination and outgrowth Bacteriocins and other microbial sources
of C. perfringens by buffered sodium citrate alone and in Antimicrobial proteins or peptides produced by bacteria
combination with sodium diacetate during abusive chilling are known as bacteriocins. These are synthesized in bacte-
of roast beef and injected pork has been evaluated by rial ribosomes and can inhibit other bacteria
Thippareddi, Juneja, Phebus, Marsden, and Kastner (Klaenhammer, 1993). Bacteriocins constitute a diverse
(2003). The incorporation of sodium citrate into roast group of antibacterial proteins that can kill closely related
beef formulation resulted in reductions in the population bacteria by various mechanisms such as by inhibiting cell
of C. perfringens by 0.98, 1.87, and 2.47 log CFU/g at wall synthesis, permeabilizing the target cell membrane,
0.5, 1.0, and 2.0% concentrations, respectively. Moreover, or by inhibiting enzyme activity (Klaenhammer, 1993).
Juneja and Thippareddi (2004) conducted the same experi- Bacteriocinsare considered as safe and effective natural
ment for ground turkey, but with two additional organic food preservatives.
acids (sodium lactate and sodium acetate). According to Nisin e a low molecular weight bacteriocin produced by
their study, sodium lactate and sodium acetate at 1% con- certain strains of Lactococcus lactis subspp. Lactis e has
centration could control C. perfringens germination and been used as a food preservative for more than 30 years.
outgrowth (<1.0 log CFU/g). Houtsma, Heuvelink, These bacteriocins have a potential for application in hurdle
Dufrenne, and Notermans (1994) showed that lactate medi- technology as effective natural preservatives (Galvaz,
ated inhibition of proteolytic C. botulinum toxin formation Abriouel, Lopez, & Omar, 2007). Fowler and Gasson
was more effective at lower temperatures, and that the (1991) demonstrated that spores of Clostridium species
44 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49

that had survived a heat treatment of 3 min at 121.1  C In addition, the effectiveness of enterocin CCM 4231 in
were ten times more sensitive to nisin. Nisin is widely controlling L. monocytogenes contamination in dry-
used as a preservative in heat processed foods as it can in- fermented salami has been examined. The addition of en-
crease the sensitivity of spores to heat in diverse species terocin resulted in the reduction of L. monocytogenes by
(Fowler & Gasson, 1991). 1.67 log cycles immediately after bacteriocin treatment
Scott and Taylor (1981) reported that 50 ppm of nisin (Laukova, Czikkova, Laczkova, & Turek, 1999).
can inhibit the outgrowth of spores of C. botulinum type The cumulative findings suggest that nisin may be
A in an agar medium; however, dosage of up to 125 ppm acceptable alternative to nitrite, or, when used as an
of nisin failed to prevent the outgrowth of these spores in adjunct, it can permit the reduction of nitrite levels in cured
cooked meat medium. Caserio, Stecchini, Pastore, and meat without compromising the safety aspects. However,
Gennari (1979) reported that 150 ppm of nitrite did not further experiments are required prior to the use of nisin
completely suppress the outgrowth of spores of C. perfrin- as a partial replacement for nitrite.
gens in frankfurters. However, a combination of 200 ppm of Apart from the natural colorants mentioned in previous
nisin and 75 ppm of nitrite could inhibit the outgrowth of sections, microbial conversion of metmyoglobin to nitrosyl-
spores. Moreover, Rayman, Airs, and Hurst (1981) found myoglobin has generated considerable interest recently. As
that 75e100 ppm of nisin in combination with 40 ppm of depicted by Table 2, several bacteria types have been tested,
nitrite could completely inhibit the outgrowth of spores of some of which demonstrated the ability of converting met-
Clostridium sporogenes in meat slurries at 37  C for 56 myoglobin to nitrosylmyoglobin, thereby providing a way
days. However, several studies evaluated the addition of ni- to produce nitrite alternatives in meat products. Bacterial
sin to meat products in order to reduce the nitrite levels nitric oxide synthase has been detected in a Nocardia spe-
(Calderon, Collins-Thompson, & Usborne, 1985; Houben cies (Chen & Rosazza, 1995) and Lactobacillus fermentum
& Krol, 1985) and found that only high level of nisin could IFO 3956 (Morita, Sakata, & Nagata, 1998). Nitric oxide is
achieve better control of C. botulinum. derived from L-arginine by the bacterial nitric oxide syn-
Enterocins at 4800 AU/g reduced the number of Listeria thase. However, it remains unclear how Staphylococcus xy-
innocua by 7.98 log cycles in cooked ham and by 9 log cy- losus can produce nitric oxide without the addition of nitrite
cles in pate. In deboned chicken breasts, 4800 AU/cm2 of and nitrate. On the other hand, we cannot assume that S. xy-
enterocins reduced the L. innocua counts by 5.26 log cycles losus contains bacterial nitric oxide synthase (Morita et al.,
as compared to that in the control. Kouakou et al. (2009) 1998). In fact, the utilization of nitrate/nitrite as an alterna-
investigated laboratory fermentation mixtures in which L. tive electron acceptor in the respiratory chain by staphylo-
monocytogenes was co-cultured at 4  C with bacteriocin- cocci seems like a possible pathway for nitric oxide
producing bacterium in lean pork meat without the addition generation. The reduction of nitrate into nitrite by S. carno-
of nitrite, and a strong antilisterial effect was noted after 1 sus has been suggested to be due to a membrane-bound ni-
week of culturing. Furthermore, enterocin AS-48 was tested trate reductase involved in respiratory energy conservation
alone or in combination with chemical preservatives against (Pantel, Lindgren, Neubauer, & Gotz, 1998). The expres-
L. monocytogenes in a cooked ham model system. AS-48 sion of nitrate reductase by staphylococci is induced by
(20, 40, and 60 mg/g) alone was active against L. monocy- anaerobic growth conditions, and the expression level is
togenes, whereas the antilisterial effect was improved the highest in the presence of nitrate during exponential
when AS-48 (40 mg/g) was combined with nitrite/nitrate, growth phase (Pantel et al., 1998).
pentasodium tripolyphosphate, sodium benzoate or potas-
sium sorbate. The most effective combination was deter- HHP treatment
mined to be AS-48-nitrite/nitrate (0.007%) because it During HHP treatment, packaged food is placed inside a
could reduce listeria counts below detection level pressure vessel and subjected to water pressure from 100 to
throughout the storage period (Ananou et al., 2010). 900 MPa, which is isostatically transmitted inside the

Table 2. Major bacteria species associated with conversion of metmyoglobin to nitrosylmyoglobin in different studies.

Microorganisms Growth mediums References

Chromobacterium violaceum Microbiological media Arihara et al. (1993)
Kurthia sp.
Lactobacillus fermentum Smoked fermented sausages Moller, Jensen, Skibsted, and Knochel (2006)
Lactobacillus fermentum Chinese style sausage Zhang, Kong, and Xiong (2007)
Pediococcus acidilactici Broth medium Gundogdu, Karahan,& Cakmakc (2006)
Lactobacillus plantarum
Staphylococcus xylosus Broth medium Morita et al. (1998)
Raw meat batters Li, Kong, Chen, Zheng, and Liu (2013)
Staphylococcus carnosus, Staphylococcus Sausages Gotterup et al. (2008)
simulans, Staphylococcus saprophyticus
 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49 45

pressure vessel. This treatment affects the cellular meta- 1.5% and 3% of salt was found to reduce the microbial
bolism and membrane integrity of food microflora counts to <2 log CFU/g at the end of storage period.
(Rendueles et al., 2011). HHP does not inhibit or destroy Pietrzak et al. (2007) revealed that a reduction in the
any unique cellular site or cell function; however, cell death quantity of added salt and sodium nitrite did not significantly
occurs due to multiple internal cell damage including ion affect the microbiological quality of cooked pork ham over 8
exchange modifications and changes in the fatty acid weeks of storage 4e6  C because HHP treatment (600 MPa,
composition, ribosome morphology, cell morphology, pro- 31  C, 6 min) achieved the same antimicrobial ability as that
tein denaturation, and inhibition of enzyme activity of salt and sodium nitrite alone. These results indicate that
(Simpson & Gilmour, 1997). HHP treatment can significantly improve the shelf-life of
Meat products must be subjected to sufficient hurdles in vacuum-packed ham, including the hams with reduced level
order to inhibit the growth of pathogenic or spoilage micro- of curing ingredients in brine. Myers et al. (2013) deter-
organisms. Specifically, the combination of high pressure mined the effect of nitrite and HHP on the growth of L.
with another hurdle technique can result in a synergy be- monocytogenes on ready-to-eat sliced ham. The use of
tween the different hurdles and thereby improve the inhib- HHP at 600 MPa for 3 min resulted in an immediate reduc-
itory effect. HHP has been used for the inactivation of tion of 3.9e4.3 log CFU/g in the L. monocytogenes popula-
pathogens in food items, including meat products, without tions. Hayman, Baxter, O’Riordan, and Stewart (2004)
affecting the flavor of foods to a large extent (Cheftel & investigated the feasibility of using HHP to extend the
Culioli, 1997). Moreover, Cheftel and Culioli (1997) sug- shelf-life and improve the safety of refrigerated ready-to-
gested the existence of a synergy between salt and HHP re- eat meats containing salt and sodium nitrite. They found
sulting from the pressure sensitization of bacterial cells, that HHP treatment at 600 MPa and 20  C for 180 s was suf-
thereby limiting their regrowth. ficient to control the levels of aerobic bacteria, anaerobic
HHP is a novel non-thermal preservation technique with bacteria or lactobacilli to below the detectable limits or at
immense potential for ensuring microbiological safety, lower levels over 95 days of storage at 4  C.
while simultaneously maintaining the sensory quality of Presently several scientists are studying HHP treatment
the food. In fact, the use of HHP could allow limiting of as an alternative approach to inactivate C. botulinum spores.
the amounts of salt and nitrite added to the meat products The effects of HHP under diverse temperature-time combi-
for prolonging their shelf-life. The feasibility of HHP appli- nations on the inactivation of spores of C. botulinum type A
cation in low-salt meat products has been investigated in phosphate buffer has also been reported by Reddy,
(Omana, Plastow, & Betti, 2011; Pietrzak, Fonberg- Solomon, Tetzloff, and Rhodehamel (2003) and Reddy,
Broczek, Mucka, & Windyga, 2007). Duranton, Guillou, Tetzloff, Solomon, and Larkin (2006).
Simonin, Cheret, and Lamballerie (2012) studied the The combined effect of HHP (200 MPa for 10 min and
response of spoilage bacteria to high pressure treatment 400 MPa for 10 min) and enterocin LM-2 (256 and 2560
in combination with different concentrations of salt and ni- AU/g) on the refrigerated shelf-life of sliced cooked ham
trite. This study demonstrated the combined effect of high has been evaluated (Liu et al., 2012). The combination of
pressure (up to 500 MPa a 20  C for 6 min) with sodium HHP (400 MPa) and enterocin (256 or 2560 AU/g) was
chloride (0e3%) or sodium nitrite (0e100 ppm) on the found to inhibit the growth of L. monocytogenes and Salmo-
outgrowth of endogenous flora of pork meat, including aer- nella Enteritidis in sliced cooked ham up to undetectable
obic mesophiles, lactic acid bacteria (LAB), and Enterobac- levels and to extend the shelf-life of refrigerated sliced
teriaceae members; a combination of high pressure with ham to 70 or 90 days, respectively. Table 3 reveals further

Table 3. Microbial inactivation by high hydrostatic pressure (HHP) alone and combined preservation treatments in meat products.

Treatment Product Effect Reference

HHP at 600 MPa Dry cured ham Absence of L. monocytigenes after 120 days Hugas, Garriga, and
Monfort (2002)
HHP at 400 MPa Cooked ham 1.9 log CFU/g reduction of L. monocytogenes after Aymerich, Jofre, Garriga,
42 days and Hugas (2005)
HHP at 450 MPa Iberian ham 3.6 log CFU/g reduction of L. monocytogenes after Morales, Calzada, and
60 days Nunez (2006)
HHP at 400 MPa Meat homogenates L. monocytogenes was < 102 CFU/g for 61 days Garriga, Aymerich, Costa,
with pediocin, Monfort, and Hugas (2002)
sakacin and enterocin
HHP at 400 MPa Sliced cooked ham Inhibition of L. monocytogenes and Salmonella Aymerich et al.(2005)
with potassium lactate during 84 days
HHP at 600 MPa Cooked ham, dry cured Listeria monocytogenes, Salmonella enterica, Jofre, Aymerich, Grebol,
ham and marinated beef loin Staphylococcus aureus below the detection limit and Garriga (2009)
during 120 days storage
46 A.U. Alahakoon et al. / Trends in Food Science & Technology 45 (2015) 37e49

findings related to microbial inactivation in meat products Apostolidis, E., Kwon, Y. I., & Shetty, K. (2008). Inhibition of Listeria
by HHP alone or in combination with other hurdles. monocytogenes by oregano, cranberry and sodium lactate
combination in broth and cooked ground beef systems and likely
mode of action through proline metabolism. International Journal
Conclusion of Food Microbiology, 128, 317e324.
Nitrite is considered as a multifunctional food additive Arihara, K., Kushida, H., Kondo, Y., Itoh, M., Luchansky, J. B., &
Cassens, R. G. (1993). Conversion of metmyoglobin to bright red
in meat curing. Several studies have indicated that nitrite
myoglobin derivatives by Chromobacterium violaceum,
intake should be limited owing to its potential carcinogenic Kurthiasp., and Lactobacillus fermenturn JCM1173. Journal of
effect in humans. In contrast, some studies have elucidated Food Science, 58(1), 38e42.
the beneficial effect of nitrite on human health; however, Aymerich, T., Jofre, A., Garriga, M., & Hugas, M. (2005). Inhibition of
the consumer demand for natural or nitrite-free meat prod- Listeria monocytogenes and Salmonella by natural antimicrobials
and high hydrostatic pressure in sliced cooked ham. Journal of
ucts remains high. Hence, the challenge for the meat indus-
Food Protection, 68(1), 173e177.
try is to search for effective strategies to reducing the Balentine, C. W., Crandall, P. G., O’Bryan, C. A., Duong, D. Q., &
residual nitrite in cured meat and to search for better alter- Pohlman, F. W. (2006). The pre- and post-grinding application of
natives for nitrite for the preparation of uncured/naturally rosemary and its effects on lipid oxidation and color during storage
cured meat products. Emerging technologies such as HHP of ground beef. Meat Science, 73(3), 413e421.
Bergamaschi, M., & Pizza, A. (2011). Effect of pork meat pH on iron
and several plant-based extracts, microbial sources, and
release from heme molecule during cooking. Journal of Life
organic acids can be effectively used in processed meats Science, 5, 376e380.
as nitrite alternatives. However, no single substitute for ni- Bisha, B., Weinsetel, N., Brehm-Stecher, B. F., & Mendonca, A.
trite is available that can simultaneously provide all the (2010). Antilisterial effects of gravinol-grape seed extract at low
functions of nitrite. Therefore, the most effective approach levels in aqueous media and its potential application as a produce
wash. Journal of Food Protection, 73, 266e273.
is to use hurdle technologies for meat curing, in which low
Brewer, M. S., Rostogi, B. K., Argoudelis, L., & Sprouls, G. K. (1995).
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compounds and/or with other processing technologies pos- and color of aerobically packaged ground pork. Journal of Food
sessing inhibitory activities against the most prevalent path- Science, 60(1), 58e62.
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