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Comparing Innovative Versus Conventional Ham Processes via Environmental Life Cycle Assessment Supplemented with the Assessment of Nitrite Impacts on Human Health

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Global sustainability indicators, particularly in human health, are necessary to describe agrifood products footprint. Nitrosamines are toxic molecules that are often encountered in cured and processed meats. As they are frequently consumed, meat-based products need to be assessed to evaluate their potential impact on human health. This article provides a methodological framework based on life cycle assessment for comparing meat product processing scenarios. The respective contributions of each step of the product life cycle are extended with a new human health indicator, nitrosamine toxicity, which has not been previously included in life cycle assessment (LCA) studies and tools (software and databases). This inclusion allows for the comparison of conventional versus innovative processes. Nitrosamines toxicity was estimated to be 2.20x10−6 disability-adjusted life years (DALY) for 1 kg of consumed conventional cooked ham while 4.54x10−7 DALY for 1 kg of consumed innovative cooked ham. The potential carcinogenic and noncarcinogenic effects of nitrosamines from meat products on human health are taken into account. Human health indicators are an important step forward in the comprehensive application of LCA methodology to improve the global sustainability of food systems.
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applied
sciences
Article
Comparing Innovative Versus Conventional Ham Processes via
Environmental Life Cycle Assessment Supplemented with the
Assessment of Nitrite Impacts on Human Health
Gaëlle Petit 1, * , Gina Villamonte 1,2, Marie de Lamballerie 1and Vanessa Jury 1


Citation: Petit, G.; Villamonte, G.;
de Lamballerie, M.; Jury, V.
Comparing Innovative Versus
Conventional Ham Processes via
Environmental Life Cycle Assessment
Supplemented with the Assessment
of Nitrite Impacts on Human Health.
Appl. Sci. 2021,11, 451.
https://doi.org/10.3390/app11010451
Received: 18 November 2020
Accepted: 24 December 2020
Published: 5 January 2021
Publisher’s Note: MDPI stays neu-
tral with regard to jurisdictional clai-
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Copyright: © 2021 by the authors. Li-
censee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Oniris, Universitéde Nantes, CNRS, GEPEA, UMR 6144, F-44000 Nantes, France;
Gina.Villamonte@celabor.be (G.V.); marie.de-lamballerie@oniris-nantes.fr (M.d.L.);
vanessa.jury@oniris-nantes.fr (V.J.)
2CELABOR, Food Technologies Nutrition Department, Avenue du Parc 38, 4650 Herve, Belgium
*Correspondence: gaelle.petit@oniris-nantes.fr
Featured Application: Both methodological in developing LCA with human health indicators
and applied in highlighting the interests of high-pressure technologies on the one hand and
alternatives to nitrites in ham on the other hand.
Abstract:
Global sustainability indicators, particularly in human health, are necessary to describe
agrifood products footprint. Nitrosamines are toxic molecules that are often encountered in cured
and processed meats. As they are frequently consumed, meat-based products need to be assessed to
evaluate their potential impact on human health. This article provides a methodological framework
based on life cycle assessment for comparing meat product processing scenarios. The respective
contributions of each step of the product life cycle are extended with a new human health indicator,
nitrosamine toxicity, which has not been previously included in life cycle assessment (LCA) studies
and tools (software and databases). This inclusion allows for the comparison of conventional versus
innovative processes. Nitrosamines toxicity was estimated to be 2.20x10
6
disability-adjusted life
years (DALY) for 1 kg of consumed conventional cooked ham while 4.54x10
7
DALY for 1 kg
of consumed innovative cooked ham. The potential carcinogenic and noncarcinogenic effects of
nitrosamines from meat products on human health are taken into account. Human health indicators
are an important step forward in the comprehensive application of LCA methodology to improve the
global sustainability of food systems.
Keywords: life cycle assessment (LCA); Nitrosamines; Nitrites; Meat product; Innovative process
1. Introduction
1.1. Sustainability Impact Assessment in the Agrifood Industry and Meat Sector
Food accounts for 20% to 30% of the environmental impact of total household con-
sumption in the European Union and could contribute more than 50% of some impact
categories, such as the acidification impact category. Meat products are partly responsible
for this high environmental impact [
1
]. Pork (fresh meat and sausage) was still the most
consumed meat in 2015 worldwide, with a consumption rate of 15.3 kg/per year in carcass
equivalents, representing approximately 37% of the total meat consumption [
2
]. Pork offers
a wide variety of products at a low price and is fairly stable, and 34% of meat product vol-
umes were purchased in a processed form [
3
]. Ham production has, therefore, significant
impacts on human health and the environment.
Much work has been done on the environmental assessment of meat production
through life cycle assessment (LCA) studies. For example, in a Weidema study [4], house-
hold storage accounted for 20% of the total energy consumption in the life cycle of meat
products. Calderon et al. [
5
] identified transportation as a second priority step in the
Appl. Sci. 2021,11, 451. https://doi.org/10.3390/app11010451 https://www.mdpi.com/journal/applsci
Appl. Sci. 2021,11, 451 2 of 18
environmental impact of canned pork. According to Davis and Sonnesson [
6
], reducing the
environmental impact of eating a poultry-meat-based meal is as important as improving
the environmental performance of manufacturing a ready-to-eat product. Some improve-
ments have been proposed in three aspects of the life cycle of meat products: utilization
(reducing food waste transportation), agricultural steps (reducing water use and emissions
to the environment, as well as land use), and energy consumption (reducing agricultural
consumption, food processing, distribution, and household consumption) [4].
However, most studies still stop at the farm gate [
7
9
]. Life cycle steps occurring
before the farm gate (livestock feed and animal husbandry) are mainly responsible for the
total environmental impact, with over 80% contribution to acidification and eutrophication
and 60% to 80% contribution to greenhouse gas emissions [
4
,
10
13
]. The life cycle steps
after the farm gate (slaughter, production, distribution, and consumption) account for
10% to 40% of greenhouse gas emissions and 10% to 70% of energy consumption, with
a very small contribution to acidification and eutrophication impacts [
4
,
6
,
7
,
10
12
,
14
18
].
On the other hand, water depletion has been recently included in LCA studies of meat
products as an impact category. The contribution of the post-farm steps to this category is
15–36% [
19
21
], depending on the species; for example, the contribution of the post-farm
steps to the carbon footprint of packaged fresh beef is negligible [22].
The contribution of life cycle steps to the global impact of the product is then influ-
enced by the specific characteristics of the meat (species, energy sources, type of processing,
packaging, storage, transport, and consumption mode) and the methodological choices of
the studies (system limits, type of allocation, and assumptions). These conditions prevent
the comparison of environmental impacts between products. Other discriminating indi-
cators are still needed to better characterize and compare the sustainability of products.
This is why this study focuses on a human health indicator, based on nitrosamines from
nitrites in ham. Those substances have been selected because they are largely discussed in
the literature [23].
1.2. Human Health Footprint: The Case of Nitrosamines in Ham Production
Meat products may contain nitrites that are used for their technological role (color and
oxidation prevention), sensory attributes, and preservation of those products. Nitrites are
precursors of nitrosamines: nitrosamines are formed from the reaction between nitrites
and amino acids or secondary amines. Nitrosamines are molecules with known toxicity,
especially their carcinogenic effects. In the environment, the main sources of nitrosamines
are food, cigarettes, and occupational activities (rubber manufacturing), and they are thus
pollutants of water sources [
24
,
25
]. Indeed, an exposure pathway is the consumption of
meat products [
26
]. This is why the authorized amount of sodium nitrite in meat products
is regulated and limited to a maximum of 150 mg.kg
1
product [
27
] by the European Food
Safety Authority (EFSA).
The nitrosamines most commonly found in the meat matrix are N-nitrosodimethylam-
ine (NDMA), N-nitrosodiethylamine (NDEA), N-nitrosopiperidine (NPIP), and N-nitrosop-
yrrolidine (NPYR) [
28
]. Among these substances, NDMA and NDEA are recognized as
probable carcinogens by the International Agency for Research on Cancer (IARC) [2931].
NPIPs and NPIYRs also have the potential to pose cancer risks. However, some agents,
such as ascorbic acid and alpha-tocopherol, influence the reaction and decrease the forma-
tion of nitrosamines.
Daily consumption of nitrites may increase the risk of gastrointestinal cancer due to
the
in vivo
formation of nitrosamines. The endogenous formation of N-nitroso compounds
in the stomach is complex and depends on several factors, such as gastric pH, bacteria,
and the presence of antioxidants [
32
]. The amount of those components is therefore very
complex to evaluate, model, and predict [
33
]. In addition, the processing and storage of
meat can increase the amount of amines available for nitrosamine formation [
34
]. Therefore,
many alternatives have been developed to limit the use of nitrites in cured and processed
Appl. Sci. 2021,11, 451 3 of 18
meat products [
35
]. Figure 1illustrates the general risks and benefits associated with nitrite
treatment of ham and, more generally, of cooked and processed meat products.
Appl. Sci. 2021, 11, x 3 of 19
and processed meat products [35]. Figure 1 illustrates the general risks and benefits asso-
ciated with nitrite treatment of ham and, more generally, of cooked and processed meat
products.
Cooked ham has been widely used as a marker of the exposure of nitroso compounds
because it is largely consumed, and thus exposure to nitrosamines could be considered
significant [36–39].
Figure 1. Overview of the risks and benefits associated with nitrite addition to processed meat.
1.3. High-Pressure Treatment: A Scenario to Reduce Nitrite Content
Because of the potentially harmful effect of nitrites, new technologies have been de-
veloped to decrease or eliminate nitrite contents in meat products. High-pressure treat-
ment represents a promising alternative to the addition of nitrites in ham due to its preser-
vation ability during the life of the product. The resistance of bacteria in the food medium,
as well as the recovery of bacterial activity after pasteurization, are two major problems
in meat products. It was shown in 1895 that starting from 400 MPa a high-pressure treat-
ment could significantly slow down the growth recovery of microorganisms, such as
weathering or pathogenic bacteria. It thus increases the shelf life of the products [40–43].
Deactivation depends on many parameters, such as the type of pathogen, pressure level,
process temperature, treatment time, and pH. For example, some studies have shown that
a storage temperature lower than 6 °C, combined with a treatment of 600 MPa, can prevent
the resumption of growth of Listeria monocytogenes in cooked ham [44,45]. High-pres-
sure treatment cannot always replace conventional techniques but may be a complemen-
tary treatment that increases the shelf life of meat products. Currently, meat products rep-
resent 30% of high-pressure products marketed [46], and high-pressure cooked ham is
one of the first products marketed in Europe at the end of the nineteenth century [47].
The addition of a high-pressure operating unit in ham production could have an ef-
fect on the environmental impact of the final product and especially on human health
consequences. Therefore it seemed important to discriminate between the different pro-
cesses and to evaluate the environmental and human health impacts of the life cycle of
cooked ham. The environmental performance of high-pressure processing technology for
food processing was compared with traditionally used food preservation technologies
such as thermal pasteurization and modified atmosphere packaging [48]. Based on the
methodology of life cycle analysis, involving in particular primary data on the flows and
consumption of high-pressure processing (HPP) plants, the evaluation of the environmen-
tal performance of sliced Parma ham shows that high-pressure treatment appears to have
a lower environmental impact in almost all impact categories than others processes. In-
deed, packaging under a modified atmosphere requires a large amount of packaging ma-
terials and food gases, and thermal pasteurization a large amount of energy. This study
aims to highlight the environmental benefits of high-pressure treatment, a well-known
non-thermal technology, but still limited in terms of use. Further studies confirming its
Figure 1. Overview of the risks and benefits associated with nitrite addition to processed meat.
Cooked ham has been widely used as a marker of the exposure of nitroso compounds
because it is largely consumed, and thus exposure to nitrosamines could be considered
significant [3639].
1.3. High-Pressure Treatment: A Scenario to Reduce Nitrite Content
Because of the potentially harmful effect of nitrites, new technologies have been
developed to decrease or eliminate nitrite contents in meat products. High-pressure
treatment represents a promising alternative to the addition of nitrites in ham due to its
preservation ability during the life of the product. The resistance of bacteria in the food
medium, as well as the recovery of bacterial activity after pasteurization, are two major
problems in meat products. It was shown in 1895 that starting from 400 MPa a high-pressure
treatment could significantly slow down the growth recovery of microorganisms, such as
weathering or pathogenic bacteria. It thus increases the shelf life of the products [
40
43
].
Deactivation depends on many parameters, such as the type of pathogen, pressure level,
process temperature, treatment time, and pH. For example, some studies have shown that
a storage temperature lower than 6
C, combined with a treatment of 600 MPa, can prevent
the resumption of growth of Listeria monocytogenes in cooked ham [
44
,
45
]. High-pressure
treatment cannot always replace conventional techniques but may be a complementary
treatment that increases the shelf life of meat products. Currently, meat products represent
30% of high-pressure products marketed [
46
], and high-pressure cooked ham is one of the
first products marketed in Europe at the end of the nineteenth century [47].
The addition of a high-pressure operating unit in ham production could have an
effect on the environmental impact of the final product and especially on human health
consequences. Therefore it seemed important to discriminate between the different pro-
cesses and to evaluate the environmental and human health impacts of the life cycle of
cooked ham. The environmental performance of high-pressure processing technology for
food processing was compared with traditionally used food preservation technologies
such as thermal pasteurization and modified atmosphere packaging [
48
]. Based on the
methodology of life cycle analysis, involving in particular primary data on the flows and
consumption of high-pressure processing (HPP) plants, the evaluation of the environmental
performance of sliced Parma ham shows that high-pressure treatment appears to have a
lower environmental impact in almost all impact categories than others processes. Indeed,
packaging under a modified atmosphere requires a large amount of packaging materials
and food gases, and thermal pasteurization a large amount of energy. This study aims to
highlight the environmental benefits of high-pressure treatment, a well-known non-thermal
technology, but still limited in terms of use. Further studies confirming its low impact on
the environment are required and should be supplemented with human health analyzes.
Appl. Sci. 2021,11, 451 4 of 18
In this article, a combination of two innovative processes was evaluated, high-pressure
processing and biopreservation with lactic acid bacteria, as recommended by Simonin
et al. [
49
]. The objectives of this study were the following: (i) comparison of the poten-
tial environmental impact of ham production through two different technological paths:
conventional production versus production with an innovative process (high pressure +
biopreservation); (ii) development of a characterization factor to take into account nitrite
contents in the human health impact and to help compare different technological processes.
2. Methods
2.1. Environmental Life Cycle Footprint of Ham Production
Goal and scope: The reference system corresponded to the production of a conven-
tional, superior ham.
Functional unit: The main function of cooked ham is to feed the population by meeting
implicit and/or explicit consumer needs. Cooked ham is mainly sold sliced, and the weight
of the unit of sale most often purchased is 0.18 kg (or four slices). For our study and to
compare alternative systems, all emissions and resources are linked to a reference quantity
of product. The functional unit was defined as “1 kg of consumed cooked ham”, i.e.,
superior ham than that mainly consumed in France, namely free of polyphosphates like in
Rakotondramavo et al. [50].
System boundaries: The system boundary determination was based on the methodol-
ogy presented by Hospido et al. [
51
]. The following four steps were modeled: raw material
production, cooked ham production, distribution, and use phase (consumption). The
raw material production stage included conventional breeding (birth, postweaning, and
fattening) of pigs in France. The elements included in the subsystem were energy and water
production, livestock infrastructure, and feed production. However, veterinary products,
cleaning products, food distribution, power cables, and infrastructure for the production
of food were not included. The cooked ham production stage included transportation of
live pigs to the slaughterhouse, slaughtering and cutting operations (electrical stunning,
scalding, dehairing, buckling, eviscerating, bleeding, and cutting), refrigerated transport
to the slaughterhouse ham production plant, and cooked ham production operations
(receiving, deboning, brining, molding, baking, cooling, slicing, packaging, storing and
transporting the ingredients, and primary packaging). The annual production data at the
slaughterhouse are related to the quantity of ham pieces per mass allocation. The transport
distance between groups of pork producers from the Brittany region and the slaughter-
house was estimated by weighting according to the regional distribution of production.
Slaughter-cutting waste accounts for 15% of the live pig weight [
52
]. The production plant
also produces other meat products. The annual production data at the plant were related
to the quantity of cooked ham per mass allocation. This study considered the absence
of losses during the production of ham. This study also excluded the manufacture of
additives (sodium ascorbate and aromatics) present in the processing of the product as
well as their transport because they represent less than 0.1% of the final composition of
the product. The infrastructure of the facilities, equipment, packaging used for temporary
storage and products used for cleaning the facilities were not included. The influence of
combined biopreservation and high-pressure processing was evaluated in terms of the
life cycle of cooked ham from data on an industrial scale to assess the human health and
environmental impacts of its potential application. In the conventional ham production
scenario, an embedded amount of 0.1 g per kilo of nitrites was included. No nitrites were
assumed to be used in the innovative scenario. A high-pressure program of 600 MPa
for 3 min at room temperature was used in this study (data from Villamonte 2014 [
53
],
and from a confidential report disclosed by Hiperbaric). A spray of 25 mg of commercial
lactic starter slurry per kilo of ham was used for the biopreservation of the product. Bio-
preservation is based on the principle of using natural microbial cultures to avoid food
spoilage and increase food security. The ferments, therefore, tend to lengthen the shelf life
of food by avoiding product degradation. The cultures of lactic ferments used for ham
Appl. Sci. 2021,11, 451 5 of 18
are specially developed for food application. The extension of the lifetime associated with
this innovative treatment (60 days) is comparable to that associated with the conventional
treatment product [
54
,
55
]. This process did not alter the rest of the life cycle of the product
(distribution or consumption, for example). The distribution stage included transport from
the plant’s warehouses to the distribution platform, storage on the platform (two days),
transport to the supermarket, and storage time (energy consumption) in a display case
(linear) at the supermarket (seven days). The infrastructure and packaging for transport
and storage were not included. The distribution platform was estimated using the Brunel
University study approach [
56
] and information from a study by Rizet et al. [
57
]. For
point-of-sale storage, estimates were obtained from summer energy evaluation studies
of a supermarket in France. Round-trip transport with vehicles subject to the European
EURO 4 emission standard was considered. The use phase included transportation from
the supermarket to the consumer’s home, and storage of the product (seven days) in a type
A energy label refrigerator was included. The transport characteristics corresponded to an
urban consumer in France from the point of sale. The study assumed 3.15% waste of the
product, estimated according to the nature of food and waste in France [
58
]. The end of
life of the packaging waste associated with the consumption of the product was included.
The data on the energy consumption of the refrigeration were estimated according to the
model of Nielsen et al. [
52
] for a type A refrigerator. The waste was treated by incineration
with energy recovery (52.4%) or by storage (47.6%). The steps included in the limits are
shown in Figure 2.
Allocation method: mass allocation.
Inventory of inputs, emissions, and resources: The system was described and modeled
with SimaPro 8.5.0.0 software (PRéSustainability, Amersfoort, The Netherlands) [
59
]. The
life cycle inventory included the flow of materials and energy within the system boundaries,
adjusted to 1 kg of consumed cooked ham. The primary data (real) were measured and/or
provided by officials of the French pork industry French National Pork Institute (IFIP)
and a high-pressure processing equipment company (Hiperbaric in Spain). Secondary
data (from databases) were supplemented by the database and bibliography available
for the reference technology path. The specifications and modalities of the reference and
innovative processes were based on the data obtained from the partners, for example, the
high-pressure treatment schedules and the inventory of resources needed to cultivate the
preservation fermentation. The data for the raw material production step were collected
from the Agribalyse French agricultural products database (version 1.3)—the information
obtained on pig slaughtering corresponded to an average French slaughterhouse. The
data for cooked ham production were collected from conventional French meat producers.
The technological level used in the slaughtering and manufacturing steps was modern or
automated, and the site capacities were representative of French production. The generic
data originated from the EcoInvent 3.3 database. The energy source was that of France
and was acquired from this database. The quality of the related data was categorized into
generic (pig breeding, distribution, and use) and specific (slaughter-cutting, production of
cooked ham, and high-pressure treatment). This information was temporally representative
of current production technologies and consumption habits, and based on available sources:
livestock (Agribalyse V1.1 February 2014, ILCD-Quality final note 4,5/5), slaughter-cutting
and cooked ham production (from IFIP, 2014), distribution (from Villamonte, 2014 [
53
]), and
use (data from Villamonte, 2014 [
53
]). To summarize, the flows that change between the
different scenarios studied are, on the one hand, those linked to the unitary high-pressure
treatment operation (i.e., for a kg of cooked ham, 0.0695 kWh of electricity, 700 kPa of
compressed air, and 0.377 L of water), as well as the production flows of the lactic ferment
for biopreservation (taken into account in the study of raw materials for the manufacture
of the culture medium, liquid nitrogen, in particular for keeping the packaging cold,
energy and water required, emissions into the air and water (BOD and COD), reduction of
avoided impacts thanks to the spreading of the culture medium after use on land in direct
proximity to the production of the ferment).
Appl. Sci. 2021,11, 451 6 of 18
Appl. Sci. 2021, 11, x 6 of 19
Figure 2. Cooked ham life cycle (brown for raw material, blue for cooked ham production, green for distribution, and
orange for consumption).
Allocation method: mass allocation
Inventory of inputs, emissions, and resources: The system was described and mod-
eled with SimaPro 8.5.0.0 software (PRé Sustainability, Amersfoort, The Netherlands) [59].
The life cycle inventory included the flow of materials and energy within the system
boundaries, adjusted to 1 kg of consumed cooked ham. The primary data (real) were
measured and/or provided by officials of the French pork industry French National Pork
Institute (IFIP) and a high-pressure processing equipment company (Hiperbaric in Spain).
Secondary data (from databases) were supplemented by the database and bibliography
available for the reference technology path. The specifications and modalities of the refer-
ence and innovative processes were based on the data obtained from the partners, for
example, the high-pressure treatment schedules and the inventory of resources needed to
cultivate the preservation fermentation. The data for the raw material production step
were collected from the Agribalyse French agricultural products database (version 1.3)—
Figure 2.
Cooked ham life cycle (brown for raw material, blue for cooked ham production, green for distribution, and
orange for consumption).
Impact assessment: All aspects of environmental issues were divided into impact
categories. For the food industry, resource use is an essential question in the current context.
Therefore, the cumulative demand for renewable and nonrenewable energy, abiotic re-
source depletion, and water depletion were utilized as impact categories for the study.
Reference impact categories, such as climate change, acidification, and eutrophication, were
also included. The environmental impact categories were obtained by the ReCiPe method
(version 1.12), midpoint (problems), and endpoint (damages, all expressed in DALY for
human toxicity). The impact category of water depletion represented only the amount of
water used. The cumulative demand for nonrenewable energy was determined by the
cumulative energy demand method version 1.09. This method estimated the energy use in
the life cycle from renewable and nonrenewable energy resources.
The cumulative demand for energy concerned all renewable and nonrenewable energy
sources (nuclear, oil, coal, natural gas, etc.) potentially used throughout the product life
cycle. Climate change was evaluated as the concentration of substances, such as carbon
monoxide and methane, that disrupt the climate balance and contribute to the greenhouse
effect. Metal depletion represents the extraction of mineral resources (ores), expressed in
Appl. Sci. 2021,11, 451 7 of 18
kg of equivalent iron. The indicator for the acidification category was the increase in the
concentration of acidifying substances (air pollutants) causing tree dieback, expressed in
g of sulfur dioxide (SO
2
) equivalents. The eutrophication category, expressed in g of
phosphate (P) or nitrogen (N) equivalents, reflected the quantity of nutrients released
into the environment that favor the proliferation of certain species and that cause the
disruption of ecosystems. The water-depletion impact category evaluated the total amount
of freshwater (m3) used in the life cycle of cooked ham.
2.2. Human Health Footprint of Ham Production
To take into account the effect of substances in ham, such as nitrites, a new characteri-
zation factor was developed to be included in the life cycle assessment in the human health
damage category. The methodology for the development of this new characterization factor
is described below.
2.2.1. Fate and Exposure
The causal chain of the potential toxicity of nitrosamines via ingestion of meat products
containing nitrites is presented in Figure 3. In general, chemical fate includes the transport
of the substance through different environmental compartments. The fate factor associates
the emissions from a substance in compartment n with the increase of the quantity of the
substance in this compartment (air, soil, water, and food) [
60
]. The particularity of the
effect of substances, such as nitrosamines, in foodstuffs, is partly due to the mechanism of
food ingestion. In fact, the entire emission (nitrosamines formed in the food) is ingested
by the consumer. Thus, the transfer of the substance and its accumulation in another
compartment were not taken into account. Indeed, nitrosamines are formed in meat
products (exogenous nitrosamines) via the reaction of a nitrosating agent (nitrogen oxides)
with amino compounds from proteins. These nitrosating agents are derived from nitrites
and favored by heat treatments.
Appl. Sci. 2021, 11, x 8 of 19
transport of the substance through different environmental compartments. The fate factor
associates the emissions from a substance in compartment n with the increase of the quan-
tity of the substance in this compartment (air, soil, water, and food) [60]. The particularity
of the effect of substances, such as nitrosamines, in foodstuffs, is partly due to the mecha-
nism of food ingestion. In fact, the entire emission (nitrosamines formed in the food) is
ingested by the consumer. Thus, the transfer of the substance and its accumulation in an-
other compartment were not taken into account. Indeed, nitrosamines are formed in meat
products (exogenous nitrosamines) via the reaction of a nitrosating agent (nitrogen ox-
ides) with amino compounds from proteins. These nitrosating agents are derived from
nitrites and favored by heat treatments.
Figure 3. Causality chain of the potential toxicity of nitrosamines via the ingestion of food (in-
spired by Jolliet et al. 2010 [60]).
Human exposure represents only a fraction of the substance from the food trans-
ferred (nitrosamines via the ingestion pathway) to the entire human population. The po-
tential risk to human health was calculated by the probable number of cases per kg of
substance ingested by the population. The carcinogenic and noncarcinogenic effects were
estimated by toxicity data for the substance from epidemiological studies. The severity of
these effects (carcinogenic and noncarcinogenic) was expressed in terms of equivalent life
lost per case of the disease (DALY.cas-1), a unit used by the World Health Organization
[60,61]. DALY stands for disability-adjusted life years and is also frequently used precisely
in LCA via damage-oriented and/or endpoint methods, which group the impacts accord-
ing to the results in the cause-and-effect chain and clearly show the impact on a specific
category of individuals. The damage factors on human health transform kilograms of the
equivalent substance into years of healthy life lost (DALY). For the needs of this study,
the French population was considered.
The calculation of the indicator of the potential impact of the toxicity of nitrosamines
on humans was defined from the expression established by Udo de Haes [62] for the cat-
egory of oriented damage to human health (Equation (1))
𝑆𝑖 =  𝑖𝐹𝑖 × 𝐸𝐹𝑖
(1)
Figure 3.
Causality chain of the potential toxicity of nitrosamines via the ingestion of food (inspired
by Jolliet et al. 2010 [60]).
Human exposure represents only a fraction of the substance from the food transferred
(nitrosamines via the ingestion pathway) to the entire human population. The potential
risk to human health was calculated by the probable number of cases per kg of substance
Appl. Sci. 2021,11, 451 8 of 18
ingested by the population. The carcinogenic and noncarcinogenic effects were estimated
by toxicity data for the substance from epidemiological studies. The severity of these
effects (carcinogenic and noncarcinogenic) was expressed in terms of equivalent life lost
per case of the disease (DALY.cas-1), a unit used by the World Health Organization [
60
,
61
].
DALY stands for disability-adjusted life years and is also frequently used precisely in LCA
via damage-oriented and/or endpoint methods, which group the impacts according to the
results in the cause-and-effect chain and clearly show the impact on a specific category of
individuals. The damage factors on human health transform kilograms of the equivalent
substance into years of healthy life lost (DALY). For the needs of this study, the French
population was considered.
The calculation of the indicator of the potential impact of the toxicity of nitrosamines
on humans was defined from the expression established by Udo de Haes [
62
] for the
category of oriented damage to human health (Equation (1))
Si =iiFi ×EFi (1)
where Si is the impact category indicator (DALY, functional unit
1
), Fi is the intake frac-
tion (kg taken functional unit
1
), and EFi is the effect factor (DALY, kg taken
1
) of the
nitrosamine type i. The results are the aggregation of the independent estimate of each
nitrosamine compound i in the meat product.
2.2.2. Intake Fraction
The intake fraction of nitrosamine i (iF) is defined as the ingested dose of nitrosamine
i per functional unit (FU). The dose considers the concentration of nitrosamine i per unit
of food (exogenous nitrosamines). In our study, the fraction of ingested nitrosamines was
calculated from Equation (2). The concentration of nitrosamines (
µ
g.kg
1
) at the time
of ingestion was defined by the literature reviews summarized in Table 1. Nitrosamines
formed in vivo were not part of the expression.
Ii[nitrosamines taken]
FU =Nb doses
FU ×gf ood un it
dose ×[nitrosamines]
gf ood uni t
(2)
Table 1.
The concentration of nitrosamines (N-nitrosodimethylamine (NDMA), N-nitrosodiethy-
lamine (NDEA), N-nitrosopyrrolidine (NPYR), and N-nitrosopiperidine (NPIP)) in cooked hams
used to estimate the indicator.
Nitrosamines
(µg.kg1)Reference Nitrosamines
(µg.kg1)Reference
NDMA: 5.09 ±1.01
NDEA: 4.85 ±0.54
[63] (reference
scenario)
NDMA: 4.9
NDEA: 1.49
NPYR: 5.34
NPIP: 0.04
[28]
NDMA: 11.05 ±1.2
NDEA: 10.4 ±0.96
[63] (scenario with
polyphosphates)
NDMA: 2 ±0.3
NDEA: 2.9 ±0.3
NPYR: 1.8 ±0.3
[64]
NDMA: 1
NDEA: 0.37
NPYR: 3.73
NPIP: 1.79
[65]
NDMA: 2.18 ±0.62
NDEA: 0.2
NPYR: 1.75 ±0.49
NPIP: 0.05 ±0.02
[66]
2.2.3. Effect and Severity Factor
The USEtox 1.01 model [
67
,
68
] was used to calculate the characterization factors. The
USEtox characterization model is based on a consensus to address the problems asso-
ciated with the variability of human toxicity characterization model methodology [
69
].
Appl. Sci. 2021,11, 451 9 of 18
UNEP/SETAC (United Nations Environment Programme/Society of Environmental Tox-
icology and Chemistry) created this model from other models, such as CalTOx, IM-
PACT 2002 + USES-LCA, BETR, EDIP, WATSON, and Ecosense. The aim was to create a
simple model with a solid scientific basis [
69
,
70
] to obtain problem-oriented characteriza-
tion factors. The fate and exposure factors of the model were modified according to the
previously described characteristics. The effect factors of the human toxicity characteriza-
tion models for nitrosamines from the USEtox analysis were used (Table 2). These factors
represented the variation in the probability of disease from the change in nitrosamine
uptake over the course of the life of the targeted population. The unit for the potential for
human toxicity of nitrosamines was case.kg
1
. The model expresses toxicity in comparative
toxic units (CTUs).
Table 2.
Factor of the carcinogenic effects of nitrosamines (via ingestion) according to USEtox 1.01
[67,68].
CASE Nitrosamines Carcinogenic Effect Factor
(µg.kg1Intake)
62-75-9 N-nitrosodimethylamine 11.95
55-18-5 N-nitrosodiethylamine 43.25
930-55-2 N-nitrosopiperidine 3.01
100-75-4 N-nitrosopyrrolidine 1.57
The effect factor is based on the extrapolation of ED50 (lethal dose for 50% of a
given population). The carcinogenic effects were obtained from the Carcinogenic Potency
Database. As the dose-response curve was linear, the EF (case.kg
1
taken) was calculated
according to Equation (3) [67]:
EF =0.5
ED50
(3)
To evaluate the significance of the indicator in relation to other indicators of the
damage-oriented impact category of human health from the life cycle analysis of cooked
ham, the severity factor for the carcinogenic effect of nitrosamines was considered 11.5
DALY.case-1 according to the study conducted by Huijbregts et al. [
71
] on carcinogenic
chemicals, including nitrosamines.
3. Results and Discussion: Environmental and Human Health Impact Assessment of
Cooked Ham Production
3.1. Environmental Life Cycle Assessment of Cooked Ham Production
Table 3shows the potential environmental impact results of the life cycle of cooked
ham production for conventional and innovative scenarios.
Table 3.
Environmental and human health impact of the cooked ham life cycle for conventional and
combined innovative processes. DALY: disability-adjusted life years.
Impact Category Units Conventional Ham Innovative Ham
Nonrenewable MJ-Eq 103.003 104.472
Renewable MJ-Eq 72.429 72.429
Climate change kg CO2eq 13.422 13.439
Water depletion m310.958 11.465
Metal depletion kg Fe eq 0.276 0.277
Terrestrial acidification kg SO2eq 0.084 0.086
Freshwater eutrophication kg P eq 0.001 0.001
Marine eutrophication kg N eq 0.021 0.021
Agricultural land occupation
m25.437 5.438
Human toxicity kg 1,4-DB eq 0.111 0.112
Nitrosamines toxicity DALY 2.20x1064.54x107
Appl. Sci. 2021,11, 451 10 of 18
The production of conventionally cooked ham in this study used approximately
103 MJ of nonrenewable energy for the conventional scenario and approximately 104 MJ
of nonrenewable energy for innovative scenarios. For both scenarios, the impact of 63%
was fossil energy, and 37% was nuclear energy. Conventionally cooked ham has an
impact on greenhouse gas emissions of 13.4 kg CO
2
eq.kg
1
for both scenarios (13.422
for the conventional scenario and 13.439 for the innovative scenario). The conventionally
cooked ham induced the depletion of metal resources to the order of 0.28 kg Fe eq.kg
1
of
product for both scenarios (0.276 for the conventional scenario and 0.277 for the innovative
scenario). The total amount of freshwater (m
3
) used in the life cycle of cooked ham for both
scenarios was around 11 m
3
of water (10.958 for the conventional scenario and 11.465 for
the innovative scenario).
For all impact indicators except nitrosamine toxicity, the variation between the two
scenarios was less than 5%, which is considered negligible. The potential effect of the ham
life cycle directly on human health is outlined in part 3.3 Sensitivity analysis. All of these
damage-oriented impact categories were then expressed in DALY. Effects on ecosystems
were not estimated directly in this study (but could still be calculated from problem-
oriented impact categories).
To show how similar the impacts calculated by environmental LCA are for the two
scenarios compared, Table 4presents an analysis of the contributions of the different
stages of the product life cycle. This analysis of ham life cycle hotspots shows how the
environmental life cycle analysis makes it difficult to distinguish between the two scenarios,
conventional and innovative. The production of raw material was the most important step,
accounting for 94% of the potential impact due to emissions occurring during pig farming.
Table 4.
Hotspots analysis of cooked ham life cycle impacts for conventional and innovative pro-
cesses.
Impact Category Unity Raw Material Production Production of Cooked Ham Distribution Use Phase
Conventional Innovative
Nonrenewable Energy MJ-Eq 2.81x10+1 7.08x10+1 7.24x10+1 1.98x1013.85x10
Renewable energy MJ-Eq 7.12x10+1 1.21x10 1.23x10 0.00x10 8.18x103
Climate change kg CO2eq 6.22x10 6.86x10 6.89x10 1.36x1012.02x101
Water depletion m31.50x10 8.71x10 9.22x10 1.57x1027.29x101
Metal depletion kg Fe eq 1.32x1011.24x1011.26x1014.28x1041.93x102
Terrestrialacidification kg SO2eq 6.90x1021.46x1021.69x1023.04x1054.61x104
Freshwater eutrophication kg P eq 4.42x1049.32x1049.36x1046.95x1073.29x105
Marine eutrophication kg N eq 2.00x1028.24x1049.35x1041.73x1063.28x105
Agricultural land occupation m25.15x10 2.86x1012.91x1011.33x1043.17x103
The environmental results of our life cycle analysis study on ham production are
comparable to those of previous related research. According to Carlsson–Kanyama [
10
],
the energy requirement for pork in Sweden was 32 MJ. In general, important differences
are observed between countries due to differences in the applied energy sources. These dif-
ferences with data from Sweden can therefore be explained by the different energy sources
used by the two countries. Additionally, this study considered all steps up to the point of
sale, but the product has not been treated after being slaughtered. Compared to cooked
ham, the difference is probably largely due to the extent of the contribution of ham pro-
duction and storage on the distribution and product use stages. Therefore, in our study
we considered more impacts. In addition, according to Reckmann et al. [
72
], the nonre-
newable energy demand is 19.5 MJ.kg1for slaughtered pork, with a contribution of 13%
for the slaughtering stage. In this respect, the conventionally cooked ham had a very high
energy consumption (87.7%), with a contribution of 10% from slaughtering. The breed
from the previous study conducted in Sweden was not the same type of breed that is
used in France because, according to the Agribalyse database, the nonrenewable energy
consumption for a conventional pig raised in France is equal to 17.3 MJ.kg
1
pork (live
weight). These differences originate from the processed meat product due to the high raw
material requirements (pieces of ham) and the steps required (cutting, cooking, and slicing)
to produce a superior cooked ham. Despite the importance of limiting energy demand in
sustainable food production [
73
], in the studies available on processed meat products, this
Appl. Sci. 2021,11, 451 11 of 18
impact category was not evaluated. Studies on the energy demand of meat products are
needed to identify and control or reduce the potential for preservation processes with a
high potential environmental impact.
The carbon footprint of cooked ham (13.422 and 13.439 kg CO
2
eq.kg
1
) was similar
to that obtained in other studies. In France, the carbon footprint of cooked ham was
studied by the research firm BioIntelligence Service. Their superior cooked ham had a
carbon footprint that varied from 7.71 to 8.55 CO
2
eq.kg
1
(equivalent corresponding to the
functional unit of this study) depending on the product (different numbers of slices, with or
without the rind) [
74
]. The steps taken into account in the study by BioIntelligence Service
were agriculture, manufacturing, distribution, transportation, and packaging. Between
63.1% and 75.9% of the potential for depletion of nonrenewable resources comes from the
ham production phase and, more particularly, from the raw material production phase (in
particular, pork). The consumption is mainly of electricity and gas on the farm (34.9%),
as well as the consumption of fuel on the pig farm (26.4%), which contributes the most to
the depletion of nonrenewable resources.
According to Carlsson–Kanyama [
10
], pork in Sweden has an impact of
6.1 kg CO2eq.kg1
meat (Roy et al. 2012). The CO
2
emission impacts are also dependent on the energy sources
of each country. In this case, France could be associated with low CO
2
emissions because
its electricity is predominantly nuclear. In terms of contribution, the main step was the
production of raw material, followed by packaging, cooking, transportation, slaughtering,
and storage. Distribution contributed to 3.3% of the impacts in this case. A rough esti-
mate was given by our study for the distribution stage (4%). Another study on pork pie
(
2–3 kg CO2eq.kg1
) produced in France showed that the production of raw materials also
contributed 80% of the impact to the life cycle and that the processing stage contributed
10% to the cycle. The influence of transportation was negligible [
13
]. Our results were
consistent with those of other studies: most of the impact of meat products comes from the
agricultural production stage of the raw material. With regard to the depletion of abiotic
resources, comparison with other studies on meat products was not possible because the
depletion of nonrenewable mineral natural resources was not taken into account. However,
the overall trend showed a decrease in the concentration of mineral ore [
75
]. Accord-
ing to the study by Reckmann et al. [
72
], slaughtered pork represents
57.1 g SO2eq.kg1
.
Slaughter yield and cooked ham production could be responsible for the difference in these
emissions. The important contribution of raw material production to the eutrophication
impact category was due to environmental emissions (nitrates in water and ammonia in
the air) from intensive pig farming [
76
]. The emissions from a cooked ham were at least
twice as high as those of a poultry product (19.9 to 29.9 g of PO
43
.kg
1
product, [
77
]) and
as those of slaughtered pork (23.3 g PO43.kg1product, [72]).
3.2. The Potential Impact of Nitrosamines on Human Health
This study estimated that the exposure to exogenous nitrosamines (NDMA, NDEA,
NPYR, and NPIP) by the daily consumption of cooked ham (16 g) was 0.15
±
0.11
µ
g
per day [
78
]. The variability in the product was associated with the quantification of the
various nitrite compounds. Other studies on cooked ham were limited to the estimated
NDMA concentration. For example, in our estimation, the exposure was lower than
what was reported in work by Catsburg et al. [
39
]; the contribution of exogenous nitroso
compounds was between 0 and 2.1
µ
g per day. In our study, this contribution ranged
from 0.003 to 0.34
µ
g per day and corresponded only to the consumption of cooked
ham. In addition to their use for preserving meat, nitrites are added to other foods to
preserve them by limiting the proliferation of pathogenic microorganisms, in particular,
Clostridium botulinum. Nitrates alone are used to prevent some cheeses from swelling
during fermentation. They are also naturally present in some vegetables, with the highest
concentrations occurring in leafy vegetables, such as spinach or lettuce. Moreover, these
substances can enter the food chain as environmental contaminants in water due to their use
in intensive agricultural practices, animal production and wastewater discharge. According
Appl. Sci. 2021,11, 451 12 of 18
to the European Food Safety Authority (EFSA) [
79
], based on realistic data, i.e., levels of
concentration actually observed in foods, the intake of nitrates in the form of a food additive
is less than 5% of the global exposure to nitrates through food.
The development of gastrointestinal cancer is associated with exogenous exposure to
nitroso compounds. The ingestion of exogenous nitrosamines in subjects with cancer was
0.0591
±
0.0485
µ
g per day. However, this estimate corresponds to the NDMA compound
in the diet [
80
]. Jakszyn et al. [
81
] also estimated dietary exposure to NDMA in a Spanish
population at 0.114
µ
g per day. The foods that contributed most to this exposure are
meat products (14%), beer (11%), and refined cheese (13%). In addition, a study on a
European population showed that dietary exposure to NDMA was 0.26
±
0.34
µ
g per
day and 0.19
±
0.31
µ
g per day for subjects with gastric cancer and for healthy subjects,
respectively [
82
]. The exposure determined for the consumption of cooked ham for our
study seemed high in comparison to these evaluations. However, the quantification of a
single type of nitrosamine (NDMA) causes an underestimation of the risk of exogenous
nitrosamines. In our case, the exposure to nitrosamines by the consumption of cooked
ham decreased drastically if NDMA was the only nitrite compound taken into account:
0.065
±
0.063
µ
g per day. In France, the exposure (NDMA) due to ham was estimated to be
0.0038
µ
g per day, with the presence of NDMA at 0.31
µ
g per kg ham and the annual ham
consumption of 4.45 kg during the period of 1987–1992. The exposure to NDMA in the
diet was determined to be 0.19
µ
g per day. Meat products contributed to 12.5% of NDMA
exposure [
83
]. A preliminary study estimated a daily exposure of 0.25
µ
g (NDMA) per day
per person in France [
84
]. In general, these studies only considered NDMA in assessing
nitrosamine exposure.
The exposure to preformed nitrosamines was only considered for the estimation of the
indicator. The severity of nitrosamines (2.2x10
6
DALY.kg
1
), considering the effect on an
entire population and not limited to a sensitive population, was in line with a report from
the International Agency for Research on Cancer (IARC) [
31
]. These experts recognized
that there is strong evidence to support changing the recommendations for processed meat
product consumption to achieve moderation or a reduction in consumption. Indeed, an
increased risk of colorectal cancer is associated with higher consumption of meat products.
The Global Fund for Cancer Research suggests that a reduction of 50 g meat product
consumption per day could represent a 20% decrease in the number of colorectal cancer
cases [85,86].
In regard to the human health indicators developed in this study, the potential impacts
of food safety in the use phase were not negligible. The main aim of this study was to eval-
uate the potential contribution of nitrosamines to the damage of human health throughout
the ham production life cycle. The impact on morbidity associated with contaminants
from food processes is not currently known. However, the meat production industry is
exploring alternatives to reduce or replace nitrites while preserving the microbiological
and sensory quality of the products. An innovative combination of biopreservation and
high-pressure processing has been explored to reduce nitrites in ham and contribute to
reducing the total potential human health impact by almost 8% and almost 20% for the
potential human health impact resulting from nitrosamine toxicity. Another option is the
use of plant extracts with active molecules capable of inactivating microorganisms and/or
preventing the negative effects of contaminants [
87
]. An additional option is to improve
animal nutrition in such a way as to provide substances with a beneficial effect on health
or even vitamins to react against the formation of these carcinogenic compounds [
88
,
89
].
Finally, a recent study has shown the influence of food processing conditions on the risk of
cancer. A decrease in carcinogenesis in rats was linked to the anaerobic packaging of ham
compared with unpackaged food and food exposure to air [90].
The innovative process of ham production combining high-pressure treatment and
biopreservation could be a solution to not altering the concentration of residual nitrites
in cooked ham [
91
94
]. Several high-pressure-treated meat products are marketed with
the claim “nitrites/nitrates not added”. They contain natural preservatives, such as celery
Appl. Sci. 2021,11, 451 13 of 18
juice, that replace additives conventionally used in their preservation [95]. High-pressure
microbial inactivation can allow for the production of sausages without nitrite use while
maintaining food safety [
92
,
96
]. This technology can also be used to improve the antimi-
crobial role of salt [
97
] or natural antimicrobials in ham [
44
,
45
]. Some potential impacts
on human health could be avoided by specific innovative treatments involving these new
technologies.
3.3. Sensitivity Analysis
Table 5shows the impact results of the life cycle of cooked ham production in France
in terms of damage-oriented impact categories from the ReCiPe method. All indicators are
expressed in DALY and correspond to the chosen functional unit (1 kg of ham consumed).
They describe the damage to human health attributable to each impact category.
Table 5.
Indicators of the human health impact categories of the cooked ham life cycle for two
scenarios (conventional and innovative ham).
Impact Category Units Conventional Ham Innovative Ham
Photochemical oxidant formation DALY 8.27x1010 8.29x1010
Ozone depletion DALY 2.52x1082.52x108
Ionizing radiation DALY 3.77x1083.91x108
Human toxicity DALY 7.79x1087.82x108
Nitrosamine toxicity DALY 2.20x1064.54x107
Particulate matter formation DALY 4.98x1065.08x106
Climate change DALY 1.60x1051.60x105
Climate change, particulate matter formation, and nitrosamine toxicity are major
contributors to the human health impact category. In particular, nitrosamine toxicity
presented a significant variation between the two scenarios, conventional ham versus high-
pressure processed ham. The results for conventional ham were similar to those reported
in the work of Weidema et al. [
4
]. The damage-oriented environmental impact of meat
products in the European Union was mainly due to land use (32–49%), respiratory effects
(inorganic (28–49%)), and climate change (15–23%). However, tackling the effects of
nitrosamine on human toxicity is new and thus cannot be compared with the literature.
Nitrosamines may become the third source of potential harm to human health after climate
change and particulate matter formation, with an estimated contribution of up to 10%
to the potential impacts. However, the integration of new impacts into LCAs implies a
thorough knowledge of the mechanisms that limit the development of characterization
factors [
98
]. For example, the International Agency for Research on Cancer has concluded
that ingested nitrates or nitrites are likely human carcinogens when conditions induce the
production of endogenous nitrosamines (IARC, 2010), which was not considered in this
study. This is why efforts are needed to improve the understanding of these phenomena.
Thus, the nitrosamine severity factor (11.5 DALY.cas-1) used to quantify the damage to
human health increased these uncertainties. The severity of colorectal cancer could be as
high as 8.8 DALY, and that of stomach cancer could be as high as 13.6 DALY [99].
4. Conclusions
Food safety is a predominant attribute of a product in the implicit or explicit evalua-
tion by the consumer, other stakeholders, and even the individuals involved themselves in
the product life cycle. This study aimed to propose a multicriteria LCA-based approach,
including environmental and human health indicators, to measure and compare the po-
tential effects of a food product for different processing scenarios. A conventional LCA
did not show a significant difference between two ham production scenarios, while the
addition of human health indicators allowed them to be distinguished because for all
impact indicators except nitrosamine toxicity, the variation between the two scenarios was
less than 5%, which was considered negligible.
Appl. Sci. 2021,11, 451 14 of 18
The impacts of life cycle steps on human health should be included in more food LCA
studies. Indeed, these indicators are not negligible because this study showed that the
product characteristics have a potential impact on human health that is comparable to other
sources of environmental impact. Exposure to nitrosamines comes from various sectors of
the environment. However, their presence in food is specific because the substances are
preformed and because the food is a source of the precursors that allow for their formation
in vivo
. The complexity of these mechanisms makes it impossible to establish more reliable
models to measure their total exposure and to define a more predictable degree of severity.
Additional work aimed at better understanding this mechanism is necessary. The definition
of indicators describing the potential impact of product life cycle steps on human health
makes it possible to compare and evaluate several scenarios as part of a product-process
innovation approach by highlighting the consequences of implementing such alternatives.
A separate publication dedicated to the construction of several human health indicators
linked to the addition or not of nitrites in ham will be proposed following this work. The
potential impacts of a processed ham using new technologies could then be compared to
those of a conventionally cooked ham. A comparative analysis of innovative processes as
new life cycle steps would allow us to consider changes in product quality that may have
consequences for human health and the environment.
Author Contributions:
G.P.: Conceptualization, Methodology, Investigation, Data gathering, Data an-
alysis, Writing, Original draft preparation, Reviewing and Editing; G.V.: Methodology, Data gath-
ering, Data analysis; M.d.L.: Supervision, Funding acquisition, Visualization, Validation; V.J.: Su-
pervision, Funding acquisition, Visualization, Validation All authors have read and agreed to the
published version of the manuscript.
Funding:
This research was funded by the French National Research Agency (BLacHP ANR-14-
CE20-0004).
Conflicts of Interest: The authors declare no conflict of interest.
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High-pressure processing (HPP) destroys pathogenic and spoilage organisms while keeping food chemistry basically intact and enables pasteurization of foods with minimal effects on taste, texture, appearance, or nutritional value. The principles that govern the behavior of foods under pressure include Le Chatelier's principle, principle of microscopic ordering, and isostatic principle. A typical HPP process uses food products packaged in a high-barrier and flexible pouch or a plastic container. The rapid heating and cooling resulting from HPP treatment offer a unique way to increase the temperature of the product only during the treatment, and to cool it rapidly. Sufficient time after food treatment should be allowed to confirm that sub-lethally injured organisms do not recover after validating an HPP pasteurization process.
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