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<article xmlns:xlink="http://www.w3.org/1999/xlink">
  <front>
    <journal-meta />
    <article-meta>
      <title-group>
        <article-title>A Review of the Quality and Hygiene of Sheep and Goat Meat Produced in Greece</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <string-name>Vangelis Economou</string-name>
          <xref ref-type="aff" rid="aff2">2</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Ioannis Ambrosiadis</string-name>
          <email>ambros@vet.auth.gr</email>
          <xref ref-type="aff" rid="aff3">3</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Alexandros Theodoridis</string-name>
          <xref ref-type="aff" rid="aff1">1</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Aggeliki Argyriadou</string-name>
          <xref ref-type="aff" rid="aff0">0</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Theodoros Kalitsis</string-name>
          <xref ref-type="aff" rid="aff0">0</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Georgios Arsenos</string-name>
          <email>arsenosg@vet.auth.gr</email>
          <xref ref-type="aff" rid="aff0">0</xref>
        </contrib>
        <aff id="aff0">
          <label>0</label>
          <institution>Laboratory of Animal Husbandry, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki</institution>
          ,
          <country country="GR">Greece</country>
        </aff>
        <aff id="aff1">
          <label>1</label>
          <institution>Laboratory of Animal Production Economics, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki</institution>
          ,
          <country country="GR">Greece</country>
        </aff>
        <aff id="aff2">
          <label>2</label>
          <institution>Laboratory of Hygiene of Food of Animal Origin - Veterinary Public Health, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki</institution>
          ,
          <country country="GR">Greece</country>
        </aff>
        <aff id="aff3">
          <label>3</label>
          <institution>Laboratory of Technology of Food of Animal Origin, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki</institution>
          ,
          <country country="GR">Greece</country>
        </aff>
      </contrib-group>
      <fpage>354</fpage>
      <lpage>363</lpage>
      <abstract>
        <p>Meat quality and hygiene are perquisites for the marketing of meat and meat products. The characteristics that form the quality characterisation of meat are not always perceived but can affect several factors ensuring consumer satisfaction. Contemporary situations, such as food scandals and trends, can influence the perception of some of the quality attributes of meat. Such examples are the 2013 horse meat scandal and the increased perception of intensive meat production as cruel to animals. Sheep and goat farming is an animal production sector that is highly adapted to the Greek countryside, respecting animal welfare and an economic activity supporting a large number of families. Still, information about the characterization of Greek small ruminant's meat production is poor. In this review an effort is made to summarize the characteristics of sheep and goat meat that form the quality and hygiene of meat produced and marketed in Greece.</p>
      </abstract>
      <kwd-group>
        <kwd>meat quality</kwd>
        <kwd>meat hygiene</kwd>
        <kwd>lamb meat</kwd>
        <kwd>mutton</kwd>
        <kwd>goat</kwd>
        <kwd>Greece</kwd>
      </kwd-group>
    </article-meta>
  </front>
  <body>
    <sec id="sec-1">
      <title>1 Introduction</title>
      <p>
        The quality of meat is characterized by measurable and non-measurable
characteristics that shape the consumer preferences on raw or preserved meat
        <xref ref-type="bibr" rid="ref10">(Elmasry
et al., 2012)</xref>
        . It is determined by the organoleptic characteristics, the nutritional value,
the hygiene and the technological properties of meat. The organoleptic characteristics
are appearance, colour, taste, aroma, juiciness, tenderness and texture. Nutritional
value refers to the concentration of various macronutrients (moisture, saturated and
unsaturated fat, proteins, and carbohydrates) and micronutrients (vitamins, minerals).
The quality properties of meat (water retention capacity, pH, water activity, redox
potential) are not perceived by the consumer, but describe meat quality in a measurable
way and are required for its objective characterization
        <xref ref-type="bibr" rid="ref10">(Elmasry et al., 2012)</xref>
        .
Consumer behaviour is determined by specific factors, mainly organoleptic
characteristics, such as tenderness, juiciness and colour, with the most important being
visual suitability (colour, freshness, marbling, cut), nutritional value (less fat,
nutritional information, method of production, weight, vitamin and protein
concentration), food safety (country of origin, absence of pathogenic microbes and
dioxins), and lack of residues (hormones and antibiotics)
        <xref ref-type="bibr" rid="ref25">(Krystallis et al., 2007)</xref>
        . Meat
hygiene is a perquisite for meat quality. Therefore, meat should be characterised by
the absence of toxic residues and pathogenic microbes and their toxins, as evidenced
by the influence of meat-related scandals to consumer behaviour. In the European
Union, annual meat consumption per person decreased from 21.5 kg in 1990 to 18.6
kg in 1996 when the British government reported the possible correlation of the Bovine
Spongiform Encephalopathy with the Creutzfeldt-Jakob syndrome
        <xref ref-type="bibr" rid="ref24 ref25 ref43">(Krystallis &amp;
Arvanitoyannis, 2006; Verbekee et al., 2010)</xref>
        . Hygiene risks mostly recognized by
consumers as major threats are antibiotic residues, the meat fat and cholesterol
concentration, and meat associated microbial risks like Salmonella, Escherichia coli,
microbial toxins, and prions
        <xref ref-type="bibr" rid="ref12 ref4 ref41">(Fearne et al., 2001; Vackier &amp; Verbeke, 2003;
Arvanitoyannis et al., 2004)</xref>
        .
2
      </p>
    </sec>
    <sec id="sec-2">
      <title>Goat and sheep meat production in Greece</title>
      <p>
        Small ruminants are usually reared together. It is therefore quite common to refer
to sheep and goat meat production. Comparing small ruminant’s meat production
among European countries, Greece was the fourth sheep meat producing country and
first in goat meat production
        <xref ref-type="bibr" rid="ref11">(European Union, 2020)</xref>
        . Sheep farming in Greece is
oriented towards dairy production
        <xref ref-type="bibr" rid="ref36">(Skapetas et al., 2006)</xref>
        . Meat production is an
activity that can enhance the profitability of small ruminant farms. Sheep are mostly
slaughtered as lambs (65-70%) according to the consumer preferences
        <xref ref-type="bibr" rid="ref5">(Bernabeu et
al., 2005)</xref>
        , and possibly by breeders who prefer this practice, avoiding extra dietary
costs and fat accumulation
        <xref ref-type="bibr" rid="ref3">(Arsenos and Zygoyiannis, 2005)</xref>
        . During the period 2011
to 2017 the animals slaughtered annually were 3,671,900 lambs with a total carcass
weight of 35,836 tons, 496,657 hoggets and sheep weighing 9,891 tons, 1,856,613 kids
weighing 17,325 tons and 258,295 goats weighing 5,067 tons. The weight of the
carcass did not vary significantly, with the average weight of lambs ranging from 9.61
to 9.87 kg and kids from 9.13 to 9.49 kg, whereas the weight of sheep and goats ranged
from 18.84 to 20.78 kg and from 18.84 to 20.17 kg respectively (Fig. 1).
Number
1,396,890
1,346,843
1,267,947
2,573,065
2,473,952
2,122,906
1,814,689
      </p>
      <p>LAMBS
Weight (t)
19,716
19,474
18,179
52,344
51,700
46,217
43,224
KIDS
13,257
12,433
11,723
23,491
23,251
20,044
17,075
Weight (t)</p>
    </sec>
    <sec id="sec-3">
      <title>3 Quality characteristics of sheep meat</title>
      <p>Katsaounis et al. (1996) report, among other, the average carcass performance of
lambs of Karagouniko, Serres and Boutsko breeds slaughtered at different stages of
development. They report significant variability due in part to the wide range of growth
stages. In all breeds the carcass performance was high, being 49.65% (41.8-57.5%) in
average. The muscle content was 50.55% (43.1-58%), whereas the fat content was
25.2% (9.4-41%), and bones consisted the 18.25% (12-24.5%) of the carcass.
Concerning meat composition, the total proteins were 14.8% (12.1-17.5%), total fat
was 30.3% (16.2-44.4%), and dry matter was 49.15% (38.5-59.8%). Meat water
percentage was 50.85% (40.2-61.5%), ash 3.19% (2.38-4%) and energy was 3.74
kcal/g (2.57-4.91 kcal/g) in average. When the weight exceeded the 45% of the adult
body weight, an increase in fat percentage and a decrease in muscle and bone
percentage was observed. At this stage of development, the Boutsko lambs (small
breed) still gave carcasses in the category of light carcasses (&lt;13 kg). Skapetas et al.
(2006) report similar characteristics in a study of 40 lamb carcasses of Greek mountain
breeds at various stages of development, stating that it is possible to produce heavier
carcasses with at least equal if not better characteristics, especially if the meat is sold
in cuts and not as whole carcasses. Arsenos et al. (2006) studied the composition of
mutton in polyunsaturated fatty acids at various stages of development, highlighting
the possibility of increasing the polyunsaturated fatty acids content after a diet with
Lucerne. In a similar study, Samouris et al. (2011) described the fatty acids profile of
lamb meat, stating that no statistically significant oxidation was observed after
refrigeration for up to 10 days. Tsolakidi (2007) has examined the meat-producing
characteristics of the Chios breed and reports correlation between animal sex and
colour, and chemical composition and tenderness of the meat, with female sheep
producing carcasses of inferior quality due to slower growth rate and significantly
higher fat values. The increase of carcass weight resulted to significant increase in fat,
cooking loss and tenderness of the meat.</p>
    </sec>
    <sec id="sec-4">
      <title>4 Quality characteristics of goat meat</title>
      <p>
        Goat meat is regarded lean with nutritional properties that suit the modern
nutritional requirements for lean and nutritious meat. It is generally acceptable by
consumers, especially when it originates from animals about a year old. However, it
tends to be harder and less juicy than other types of meat, while its special smell and
taste differentiates it from mutton. In terms of colour, it has a slightly lower a* price
than sheep, an attribute that is rarely perceived. The carcasses are usually smaller and
leaner than those of sheep, which has an impact on the cuts that can be performed. In
a study by Arsenos et al. (2009) the carcasses of domestic breeds weighed 9.56 kg
when slaughtered at 85 days at a live weight of 16 kg. Their nutritional status ranged
between 1.75 and 2, and the fat percentage was in average 2.13%. Fat accumulation
occurs quite slowly in goats and is important when animals approach adult body
weight. Most fat is deposited in the abdominal cavity, making the carcass appear lean
with a small amount of subcutaneous fat
        <xref ref-type="bibr" rid="ref23 ref45">(Kirton, 1988; Webb et al., 2005)</xref>
        . In terms
of tenderness and juiciness, goat meat and its products are inferior to similar sheep
meat and its products
        <xref ref-type="bibr" rid="ref35 ref39">(Tshabalala et al., 2003; Sheradin et al., 2003)</xref>
        .
      </p>
      <p>
        The taste and aroma of goat meat are complex characteristics that are affected by
breeds, age, fat percentage, tissue, sex, diet, and cooking. The characteristic odour and
taste of sheep and goat meat is mainly formed by the branched chain fatty acids (Ha
and Lindsay, 1990). Goat meat odour is attributed to 4-ethylchloanoic acid
        <xref ref-type="bibr" rid="ref27">(Madruga
et al., 2000)</xref>
        , while other fatty acids such as 4-methylctanoic, 4-methylananoic and
4ethylpetanoic acid are also involved
        <xref ref-type="bibr" rid="ref45">(Webb et al., 2005)</xref>
        . Regarding its chemical
composition, water ranges from 59.5% to 69.8%, total proteins from 17.0 to 29.2%,
fat content from 4.4 to 21.2% and ash from 0.95 to 3.4%
        <xref ref-type="bibr" rid="ref45">(Webb et al., 2005)</xref>
        . Arsenos
et al. (2009) report that goat meat from domestic breeds had a water percentage of
74.2%, total protein 19.9%, fat percentage 4.9% and ash 1.1%. Goat meat is
characterized as red meat and therefore has significant nutritional value, as it is an
excellent source of iron, with bound iron having about 5-10% higher bioavailability
than free iron
        <xref ref-type="bibr" rid="ref45">(Webb et al., 2005)</xref>
        . The goat meat iron concentration is reported to be
2.1 mg / g, which is comparable to that of lean beef (2.72 mg/g), mutton (1.74 mg/g)
and calf beef meat (1.11 mg/g). Also, vitamin concentrations, such as those of
thiamine, riboflavin and niacin, are comparable to those of beef and mutton.
      </p>
    </sec>
    <sec id="sec-5">
      <title>5 Hygiene of goat and sheep meat</title>
      <p>
        Goat and sheep meat are ranked as the type of meat least expected to be implicated
in foodborne outbreaks in Europe
        <xref ref-type="bibr" rid="ref7 ref8 ref8 ref9 ref9">(EFSA &amp; ECDC, 2015; EFSA &amp; ECDC, 2016;
EFSA &amp; ECDC, 2017)</xref>
        . During 2015 it was responsible for only one foodborne
outbreak
        <xref ref-type="bibr" rid="ref9">(EFSA &amp; ECDC, 2017)</xref>
        . In a similar study on meat hygiene in the United
States, there is no reference to goat / sheep meat
        <xref ref-type="bibr" rid="ref30">(Painter et al., 2013)</xref>
        . However, goat
/ sheep meat can be a carrier of several pathogens. EU epidemiological data for 2015
state that the samples most frequently tested positive for Listeria monocytogenes were
small ruminant’s meat samples
        <xref ref-type="bibr" rid="ref9">(EFSA &amp; ECDC, 2017)</xref>
        . Also, in 2015, of the 354
sheep meat samples tested for STEC Escherichia coli, 15.5% were positive. In just 28
samples of goat meat officially examined, four (14.3%) were positive for STEC
Escherichia coli. The main serotypes were O146, O6 and O113. Solomakos et al.
(2009) report that 0.8% of goat meat samples and 1.3% of sheep meat samples were
positive for Escherichia coli O157: H7, a serotype that is not the most common STEC.
      </p>
      <p>
        The Hellenic Food Authority (EFET) has been publishing the results of food
analyses since 2012. Among others, the concentration of dioxins is measured in small
ruminant’s meat. The annual reports indicate the detection of small concentrations of
dioxins, well below the legislation limits
        <xref ref-type="bibr" rid="ref16 ref16 ref17 ref17 ref18 ref18 ref19 ref20 ref20">(EFET, 2014; EFET, 2015; EFET 2016;
EFET, 2017, EFET, 2018; EFET, 2019)</xref>
        . Regarding monitored zoonoses, EFET reports
that the Brucella spp. prevalence ranged between 0.049 and 0.0248 % in the
eradication areas. Small ruminant meat can harbour pathogenic bacteria. Lazou et al.
(2014) report that Campylobacter spp. was detected in 274 of the 343 carcasses of
small ruminants examined (116 heifers, 110 lambs, 63 goats and 54 sheep) with
infection rates of 78.4% for heifers, 94.5% for lambs, 63.5% for goats and 72.2% for
sheep. Probably the adequate thermal processing of small ruminant meat before
consumption is reducing the possibility of Campylobacter infection, as evidenced by
the limited number of foodborne cases attributed. Gousia et al. (2011) report that the
60% of small ruminant meat samples were positive for Escherichia coli and 66.7% for
Staphylococcus aureus, with varying degrees of resistance to antibiotics. In addition,
small ruminants can be infected by Mycobacterium avium subsp. paratuberculosis, a
bacterium that has recently been implicated for Crohn's disease in humans
        <xref ref-type="bibr" rid="ref28">(McNees et
al.., 2015)</xref>
        . Regarding parasites, the prevalence of echinococcosis in small ruminant’s
meat is quite high. Varcasia (2007) reported that among 210 sheep and 190 goats
slaughtered in 2005, the infection rate was 30.4% and 14.7% respectively. Chaligiannis
et al. (2015) report that 30.28% of the examined carcasses were found positive for
echinococcal cysts, while the corresponding percentage for goats was 6.62%. The
parasitic load of goats directly affects both yield and product quality, as reported by
Arsenos et al. (2009) who have reported an increase in meat mono-unsaturated and
poly-unsaturated fatty acids in goats free from gastrointestinal parasitic parasites.
      </p>
    </sec>
    <sec id="sec-6">
      <title>6 Conclusions</title>
      <p>Greek small ruminant’s farms are mainly oriented towards dairy production. Still,
small ruminant’s meat production is of importance, since it can enhance the
profitability of the rather widespread breeding of small ruminants. The quality of meat
can play a significant role in the marketing of it. Sheep meat quality is rather variable,
with several factors affecting its characteristics and the consumer acceptance. Goat
meat is considered more compatible with modern nutritional requirements with its
acceptance by consumers hindered only by the intensity of its distinct aroma. The
hygiene of the small ruminant meat can be regarded as superior to other meat types.
Consequently, the breeding of sheep and goats in Greece must take into account the
standardization of meat production in order to produce meat of higher quality and
ensure better marketing of its products.</p>
      <p>Acknowledgments. This research has been co-financed by the European Regional
Development Fund of the European Union and Greek national funds through the
Operational Program Competitiveness, Entrepreneurship and Innovation, under the
call RESEARCH – CREATE – INNOVATE (project code: T1EDK-05479).
by post-weaning nutritional management and weight at slaughter. Meat Science
73(1):55-65. https://doi.org/10.1016/j.meatsci.2005.10.017</p>
      <sec id="sec-6-1">
        <title>Annual</title>
        <p>Report
2014.</p>
      </sec>
      <sec id="sec-6-2">
        <title>Annual</title>
      </sec>
      <sec id="sec-6-3">
        <title>Report</title>
      </sec>
      <sec id="sec-6-4">
        <title>Annual</title>
      </sec>
      <sec id="sec-6-5">
        <title>Report</title>
      </sec>
      <sec id="sec-6-6">
        <title>Annual</title>
        <p>Report
2016.
2017.
2018.</p>
      </sec>
    </sec>
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