Food Control 17 (2006) 2229

www.elsevier.com/locate/foodcont

Determination of microbiological contamination sources

during frozen snail meat processing stages
Seran Temelli

a,*

, Canan Dokuzlu b, Mehmet Kurtulus Cem Sen

Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Uludag University, Gorukle Kampusu, 16059 Bursa, Turkey
Department of Food Technology, Karacabey Technical Vocational School of Higher Education, Uludag University, Karacabey, 16700 Bursa, Turkey
Received 5 April 2004; received in revised form 6 August 2004; accepted 10 August 2004

Abstract
This study has been conducted to determine the major contamination sources during frozen snail meat processing. Seventeen
dierent control points and/or sample types (live snail, and snail meats after steaming, after shell removal, after rst boiling, after
gutting, after second boiling, after packaging and as frozen snail meat; air samples from gutting room, boiling room and packaging
room; samples from gutting counter tops, package surfaces, scissors used during processing, forks used during processing, personnel
hands, and potable water) have been examined for the enumeration of total aerobic mesophilic bacteria, coliforms, Escherichia coli,
Enterobacteriaceae, coagulase positive staphylococci, Salmonella spp., Listeria spp., and yeast and molds. From the control points
examined, raw material and environmental air were found as the primary contamination sources. Personnel hands and equipment
used were determined as the secondary contamination sources. Second boiling and freezing stages during processing were determined to reduce the overall contamination rate, and therefore had positive eects on the microbiological quality of the nal product.
Programs approving the acceptance of snails only with low initial microbial counts to the plant, giving emphasis to processing in
proper hygiene conditions with sucient sanitary applications is strongly recommended.

2004 Elsevier Ltd. All rights reserved.
Keywords: Helix pomatia; Snail; Microbiological contamination

1. Introduction
Helix pomatia (H. Pomatia) type land snail, which is
included in Gastropoda class of Mollusca phylum, is
consumed widely particularly in countries such as
France, Belgium, Germany and Italy. Land snail consumption is in increasing demand due to its high quality
protein, low fat, high calcium, magnesium and iron content, and a part of this demand is met by Turkey.
In recent years, increases have been observed in infections and intoxications due to the consumption of fresh
water produce (Goulding, 2002; Miossec et al., 2001;

Corresponding author. Fax: +90 224 442 8025.

E-mail address: seran@uludag.edu.tr (S. Temelli).

0956-7135/$ - see front matter
2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodcont.2004.08.004

Muniain-Mujika, Calvo, Lucena, & Girones, 2003;

Steinhard, Doyle, & Cochrane, 1995; Wittman & Flick,
1995). Among these, biotoxin and histamin poisoning
occurring as a result of sh and shellsh consumption,
and viral infections due to consumption of raw or under-cooked lter feeding shellsh were indicated to occur in more than 80% of the cases (Huss, 1997;
Miossec et al., 2001; Muniain-Mujika et al., 2003; Romalde et al., 2002). Outbreaks related to bacterial pathogens are reported to be observed at the rate of 35% in
shellsh including molluscan shellsh and crustaceae
(Huss, Reilly, & Embarek, 2000). In addition, 4% of
bacterial outbreak was ound to be related to fecal contamination of shellsh by pathogens such as Salmonella
for the last 25 years (Croci, Suredini, Cozzi, & Toti,
2002; Lipp & Rose, 1997).

S. Temelli et al. / Food Control 17 (2006) 2229

In general, studies on land snails were performed on

quantitation of trace elements in meat, pollution levels
caused by heavy metals and toxic chemicals, parasitic
diseases, growing and meat quality determinations
(Caklovica, Milanovic, Loncarevic, & Nedic, 1991;
Graveland & vanderWal, 1996; Ledergerber, Leadley,
Stocklin, & Baur, 1998; Reed-Judkins, Farris, Cherry,
& Cairns, 1998; Tzouros & Arvanitoyannis, 2000). In
contrast, very few studies have been carried out related
to land snail meat in Turkey. So far, we have not
encountered a study indicating the microbiological
quality of snail meat in Turkish literature, either.
Protection of quality particularly for safety during
processing, storage and marketing of food has gained
importance in Turkey, as it has in the whole world
(FAO, 1998; Finley, Robinson, & Armstrong, 1992).
The emphasis has been given to HACCP based programs for the identication and prevention of the possible microbiological risks that can originate from raw
material, processing stages, the product and from the
food plants (Bojan, 2000; Giaccone, Ferri, & Colavita,
2002; Mantovanelli, Marino, Comi, Vallavanti, & Dolzani, 2001).
In this study we aimed to investigate possible microbiological contamination sources, and their microbial
loads during the processing stages of frozen snail meat.
Identifying these points helped us to project several solutions to eliminate or minimize the problems caused by
these sources.

2. Materials and methods

2.1. Sampling procedure
Samples were taken 10 times in dierent periods from
a private fresh water snail processing plant in Bursa/
Turkey. A ow diagram of frozen snail meat processing
stages is given in detail in Fig. 1. Snail meat samples
were collected from the following eight pre-determined
processing stages: live snail, after steaming, after shell
removal, after rst boiling, after gutting, after second
boiling, after packaging and as frozen snail. Air samples
were obtained from three separate sections (from gutting room, boiling room and packaging room) of the
processing plant. In addition, samples were collected
from gutting counter tops, package surfaces, scissors
used during processing, forks used during processing
and personnel hands. All samples were kept in prechilled containers with chiller packs, and were processed
within 24 h of collection.
Twentyve grams of snail meat was sampled for the
determination of both Listeria spp. and Salmonella
spp. Ten grams of snail meat was sampled for the
determination of other microorganisms indicated in
microbiological analyses section. Samples from the

23

Receiving
(live snail)
Washing
(with potable water)
Steaming
(in steam tunnel at 105 C for 3 min)
Automatic shelled calibration
(through sieves with predetermined pore size)
Removal of meat from shell
First boiling in water
(at 100 C for 1.5 min)
Gutting
Automatic meat calibration
(through sieves with predetermined pore size)
Second boiling in water
(at 100 C for 3.5 min - meat internal temperature 85 C)
Hand packaging and weighing
Freezing
(at 20 C)
Labelling
Frozen storage
(at 20C)
Distribution (at -20 C)
Fig. 1. Flow diagram of frozen snail meat processing stages.

personnel hands were taken as follows: workers were

let to wear sterile latex gloves and 20 ml 0.1% sterile peptone water was carefully pipetted into the gloves. Hands
in gloves were massaged completely and the gloves were
carefully taken o, tied at the top and were transferred
to the laboratory in pre-chilled insulated containers with
chiller packs (De Wit & Kampelmacher, 1988). Other
samples were removed from the surface by swab method
(Diliello, 1982), where a 10 cm2 area has been swabbed
by a pre-wetted swab in 0.1% sterile peptone water,
placed and transported in the same diluent in a cooler
within an hour of sampling. All samples were diluted
up to 10 8 with 0.1% sterile peptone water and were

24

S. Temelli et al. / Food Control 17 (2006) 2229

plated using appropriate methods for the bacteria indicated in microbiological analyses section (Croci et al.,
2002; Dore et al., 2003). When sampling from environmental air, specic agar plates without lids were kept
open in a place for 15 min, where there was normal air
circulation during processing (ISO, 1986). Two hundred
milliliters of water samples were collected at dierent
intervals from potable water used at the plant in sterile
conditions (Drinking & potable water, 1997).
2.2. Microbiological analyses
2.2.1. Enumeration of total aerobic mesophilic bacteria
Plating was performed into plate count agar (PCA,
OXOID CM 325) from the prepared dilutions by spread
plate method. Colonies formed after 48 h incubation at
30 C under aerobic conditions were counted (Swanson,
Busta, Peterson, & Johnson, 1992).
2.2.2. Enumeration of coliforms
Total coliforms were determined by the three tube
most probable number (MPN) method. Lauryl sulphate
tryptose broth (LST Broth, OXOID CM451) and brillant green lactose bile (2%) broth (BGLB Broth, OXOID CM 31) were used for presumptive and
conrmed tests for coliforms, respectively. Results were
evaluated according to the MPN tables (Book of food
material inspection & analyses procedures, 1983; Harrigan & McCance, 1976).
2.2.3. Enumeration of Escherichia coli (E. coli)
E. coli was determined by the MPN method. For this,
gas positive lauryl sulphate tryptose broth tubes were
gently agitated and a loopful from this culture was
transferred to EC Broth (MERCK 10765) tubes. The
tubes were incubated at 45.5 C for 48 h and examined
for gas formation. Gas positive cultures were streaked
onto eosine methylene blue agar (EMBA, MERCK
1347) and was incubated at 37 C for 24 h. Conrmation
of E. coli was carried out by IMViC test counts were
determined in accordance to MPN table (Andrews,
1992, Chap. 3).
2.2.4. Enumeration of Enterobacteriaceae
Double layered pour plate method was used to plate
from pre-determined dilutions onto violet red bile glucose agar (VRBGA, OXOID CM 485). All of the colonies formed were counted after aerobic incubation at
37 C for 24 h (ICMSF, 1982).
2.2.5. Enumeration of coagulase positive staphylococci
Spread plate method was performed to plate from
pre-determined dilutions onto Baird-Parker agar
(BPA, OXOID CM 275) prepared by adding sterile
egg yolk tellurite emulsion (OXOID SR 54). After incubation at 37 C for 48 h, coagulase test was applied to

typical blackgrey, bright, smooth colonies with clear

zones and counts were determined accordingly. (The
oxoid manual, 1998.)
2.2.6. Presenceabsence test of Salmonella spp.
After a non-selective pre-enrichment at 37 C for 16 h
in lactose broth, samples were transferred to Rappaport-Vassiliadis enrichment broth (RV, OXOID CM
669) for selective enrichment and plates were incubated
at 42 C for 24 h. A loopful of sample was streaked onto
bismuth sulphite agar (BSA, OXOID CM 201) for selective growth, and was incubated at 37 C for 48 h.
Browngreyblack colonies surrounded by a brown
black zone and yielding metalic sheen were regarded
as typical suspect Salmonella colonies and appropriate
conrmatory tests were performed (Andrews & Hammack, 2003).
2.2.7. Presenceabsence test of Listeria spp.
Following an incubation at 30 C for 48 h in tryptic
soy broth (TSB, OXOID CM 129) for enrichment, samples were plated onto Listeria selective agar (LSA, Oxford formulation-OXOID CM 856) by spread plate
method. After incubation at 35 C for 2448 h, grey
black colonies surrounded by a black zone were evaluated as typical Listeria colonies. These typical colonies
were streaked onto tryptic soy agar (TSA, OXOID
CM 131) and incubated at 30 C for 2448 h. Gram
staining, catalase, motility and oxidase tests were applied to selected colonies for conrmation (Hitchins,
2003).
2.2.8. Enumeration of yeast and molds
From the prepared dilutions of the samples, plating
was performed by spread plate method onto rose bengal
chloramphenicol agar (RBCA, OXOID CM 549) with
chloramphenicol selective supplement. Colonies formed
at 20 C after 45 d incubation were counted (The oxoid
manual, 1998).
2.2.9. Analysis of water
For the enumeration of aerobic mesophilic bacteria,
0.1 ml from each water sample was pipetted and spread
onto plate count agar (PCA, OXOID CM 325), and
incubated for 48 h at 30 C. The MPN method was used
for the enumeration of coliforms and E. coli (Andrews,
1992, Chap. 3).
2.3. Statistical analysis
Statistical software SPSS for Windows was used for
statistical analysis. Microbial levels at processing stages
were analyzed by Friedman nonparametric repeated
measures test, and Dunns multiple comparisons test
was applied as post-test when signicant dierences were
determined (SPSS Inc., 1992).

S. Temelli et al. / Food Control 17 (2006) 2229

25

Mean, log cfu/g.

SD, standart deviation.
Mean, log MPN/g.
AE: Dierences between the processing stages demonstrated with dierent capital letters in the same column are signicant (p < 0.05).
b

SD

0.35
0
0.34
0
0.93
0
1.37
J.16
5.63 A
<2.0 B
3.02 AC
<2.0 BD
2.43 AB
<2.0 BD
2.59 AC
1.33 PC
1.55
1.70
1.79
0
1.74
1.32
1.22
1.07
3.96 A
1.95 AB
2.53 AB
<2.0 B
2.41 B
0.80 AB
1.40 B
0.83 B
0.1
0
0.23
0
0.07
0
0
0
4.84 A
<1.0 B
1.24 AB
<1.0 B
1.56 ACD
<1.0 BE
<1.0 BE
<1.0 BE
0.27
0.15
0.26
0
0.29
0
0.15
0
A
B
AB
B
AB
B
B
B
2.56
0.51
0.63
0.47
0.64
0.47
0.51
0.47
0.34
0.36
0.58
0.48
0.38
0.47
0.60
0.23
A
B
AB
B
AB
B
B
B
2.77
0.59
1.13
0.70
0.73
0.61
0.66
0.61
1.53
0.65
0.34
0.24
0.32
0.64
0.25
0.23
Ad
A
A
B
A
C
C
C
6.85
3.72
4.15
3.21
4.68
1.52
2.53
2.24
Samples
Live snail
After steaming
After shell removal
After rst boiling
After gutting
After second boiling
After packaging
Frozen snail

Meana
SD
Meana
SD
Meanc
SDb
Meana

SD

Meanc

SD

Meana

Coagulase positive
staphylococci
Enterobacteriaceae
E. coli
Coliforms
Total aerobic
mesophilic bacteria
Microorganism

Table 1
Results of the microbiological analyses of the samples (n = 10) collected during the processing stages of frozen snail meat

Average total aerobic mesophilic bacteria count in

live snails transferred to the plant was 6.85 log cfu/g.
This number was reduced to 3.21 log cfu/g and 1.52 log
cfu/g after the rst and the second boiling, respectively.
Statistically signicant dierences were found between
shell removal and rst boiling and also between gutting
and the second boiling (p < 0.001) (Table 1). In nal
products, frozen snails total aerobic mesophilic bacteria
counts were below the indicated levels of cooked crustacea and shellsh European Council Directive 93/493
EEC, 93/51 EEC values (105 cfu/g) (Harrigan, 1998),
and the Turkish manual of seafood quality control limits (1.0 107 cfu/g) (Manual of seafood quality control,
2000).
Generally, total aerobic mesophilic bacteria count is
an important indicator of hygienic quality in foods
nluturk & Turantas, 1999).
(Ekanem & Otti, 1997; U
In our study, the reduction observed in the total aerobic
mesophilic bacteria after the second boiling is related to
be a possible result of increased temperature of 85 C
reached at the center due to heat applied 100 C for
3.5 min. Application of 90 C heat for 1.5 min in the
center (Huss et al., 2000) and 99100 C for 34 min
(Tzouros & Arvanitoyannis, 2000) heat for mollusc
and shellsh, respectively, was reported as safe for
consumption. However, these temperatures are only
sucient for the destruction of vegetative forms of the
pathogens, and therefore are not the sole safety factors
for the whole production process (Huss, 1997).
Coliform counts, which was 2.77 log MPN/g in live
snail, was determinated as 0.61 log MPN/g in frozen
snail. Similarly, 2.56 log MPN/g live snail E. coli counts
were found as 0.47 log MPN/g both after second boiling
and in frozen snail meat. In statistical analysis, dierences determined between live snail and after steaming
was signicant (p < 0.001). Similar signicant dierences
were also observed between live snail counts and counts
obtained from the followed of important stages of
processing (Table 1).
In many countries in Europe, commercial shellsh are
raised in regions, categorized according to their microbiological qualities (depending on their coliform and
fecal coliform counts) (Beliae & Cochard, 1995; Dore,
Mackie, & Lees, 2003; Dosdat & de la Pomelie, 2000).
Shellsh and related seafood exposed to waters with
fecal contamination, such as sewage water, dirty water
tanks, sea and agricultural wastes, are of risk for public
health (Geary & Davies, 2003). Presence of E. coli,
which can be destroyed with a heat application of
68.3 C for 15 min in foods, is reported as an indication
of poor sanitation conditions, insucient heat applica ntion or recontamination (Formiga-Cruz et al., 2003; U
luturk & Turantas, 1999). In this study, an increase in
the coliform and E. coli counts after packaging, which

Yeast and molds

3. Results and discussion

2.01
2.67
1.91
2.30
0
1.0
0.56
1.28
0.83

Mean, log cfu/cm2.

SD, standard deviation.
Mean, log MPN/cm2.
b

2.53
2.99

1.25

1.95
1.91
0
2.13
2.28
2.30
<2.0
2.49
2.47
3.08
0
1.62
2.93
3.45
<2.0
2.08
0
0
0
0
1.0
<1.0
<1.0
1.0
0.13
0.24
0
0.63
1.54
0.66
0.47
1.50
0.20
0.45
0
0.30
2.44
1.0
0.47
1.98
4.99
5.26
0
2.10
5.48
5.73
<2.0
2.67

Samples
Gutting counter top
Personnel hands
Package surface
Scissors used during
processing
Forks used during
processing

SD
Meana
SD
Meana
SD
Meanc
SDb
Meana

SD

Meanc

SD

Meana

Coagulase positive
staphylococci
Enterobacteriaceae
E. coli
Coliforms
Total aerobic
mesophilic bacteria
Microorganism

had decreased after the second boiling, seems to be the

result of a secondary contamination caused by personnel hands (Table 2). According to our ndings, the coliform and E. coli counts obtained in this study are well
below the indicated limits for these bacteria, which are
dened in the microbiological criteria of frozen land
snails by the Turkish manual of seafood quality control
values (210 MPN/g for coliforms and 12 MPN/g for
E. coli) (Manual of seafood quality control, 2000).
The average number of Enterobacteriaceae in live
snails transferred to the plant was 4.84 log cfu/g, and it
reduced under detectable levels after initially steaming
and also after the rst boiling. Enterobacteriaceae count
dierences were found statistically signicant between
the following stages (p < 0.001): live snail and after
steaming, rst boiling and after gutting, gutting and
second boiling (Table 1).
The average number of coagulase positive staphylococci in live snails was 3.96 log cfu/g. After the second
boiling, the number was reduced to 0.80 log cfu/g. In
the nal product as frozen snails, coagulase positive staphylococci were found as 0.83 log cfu/g. An increase was
observed in staphylococci counts after shell removal.
However, there was no signicant dierence between
the counts after steaming and after shell removal
(p > 0.001) (Table 1). According to our ndings, coagulase positive staphylococci counts (103 cfu/g) obtained
in this study were found to be below the indicated
Turkish manual of seafood quality control limits
(5.0 103 cfu/g) (Manual of seafood quality control,
2000).
It is widely known that humans are the primary
sources of contamination in most of the poisonings
caused by S. aureus, where its growth is inhibited at tem nluturk
peratures under 5 C and by boiling processes (U
& Turantas, 1999). This indicates the importance of personnel hygiene. Particularly, removal of the shell by
hand is reported as the source of contamination by staphylococci (Tzouros & Arvanitoyannis, 2000). In our
study, an increase was observed in the number of coagulase positive staphylococci after shell removal.
Although statistically found as insignicant, this is still
an indicator of a secondary contamination caused by
personnel hands.
Salmonella spp., which can cause infections even with
low counts (110 cell/g), have been reported to form the
natural microora in the farms and pools of the shellsh, where they are raised, and therefore, can be a risk
factor for humans and animals (Huss et al., 2000; Martinez-Urtaza et al., 2003; Plusquellec et al., 1994). In our
study, we did not detect any Salmonella spp. from any of
the processing stages. This result is in accordance with
the European Directives criterion indicating that no
Salmonella sp. should be found in 25 g of live and
cooked crustaceae and molluscan shellsh (Harrigan,
1998), and with the Turkish manual of seafood quality

Yeast and molds

S. Temelli et al. / Food Control 17 (2006) 2229

Table 2
Results of the microbiological analyses of the samples (n = 10) collected from equipment, packaging material and personnel hands during frozen snail meat processing

26

S. Temelli et al. / Food Control 17 (2006) 2229

control values (should not be present in 25 g) (Manual of

seafood quality control, 2000).
In our study, we detected Listeria spp. in the rst
three stages of the processing. Presence of Listeria spp.
in live snail samples is an indicator of a primary contamination source from raw material in the plant. Samples
still harbored Listeria spp. after steaming. This indicates
that steaming could not entirely eliminate Listeria spp.
from the snail, possibly due to insucient heat transfer
to the center of the snails in the steam tunnel. Listeria
spp. could be detected after shell removal, but could
not be detected in samples taken after the rst boiling
and from the stages followed.
It is widely known that heat applications at 70 C for
0.32 min is sucient to destroy L. monocytogenes
(Huss, 1997; Huss et al., 2000) however there can be
recontaminations from dierent sources (Fuchs &
Nicolaides, 1994; Iida et al., 1998). Our results indicate
that there was no recontamination or cross-contamination from the aspect of Listeria spp. after the rst boiling
stage in the plant.
In this study, yeast and mold count, which was under
detectable levels, has increased to 3.02 log cfu/g after
shell removal. After packaging, this count increased to
2.59 log cfu/g, which was higher than the count determined after the second boiling. Both of these increases
observed in two cases were found signicant by statistical analysis (p < 0.001) (Table 1). The increase in the
yeast and mold counts after shell removing, gutting
and packaging can be related to secondary contaminations from environmental air and poor hygiene applied
in the plant.
Results of the microbiological analysis of samples
collected from equipment and personnel hands revealed
that counts were notably high from the aspect of total
aerobic mesophilic bacteria, E. coli and coagulase positive staphylococci (Table 2). This may be an indication
of insucient sanitary applications in the plant (Marriott, 1999).
Packaging material is an important contamination
and/or recontamination source particularly for S. aureus
(Huss, 1997; Tzouros & Arvanitoyannis, 2000). However, in this study, analysis of the samples taken from
the packaging material revealed that there was no
microbial risk related to this material.
Environmental air, which considered as an important
quality criterion in open air exposed, cold processed and
frozen foods, is an important factor for microbial, particularly yeast and mold contamination (Huss, 1997; Tukel & Dogan, 2000). Therefore in our study we have
sampled air from three separate sections of frozen snail
meat processing plant and analyzed these samples for
total aerobic mesophilic bacteria and yeast and molds.
Overall, all three of the rooms had 2.673.82 log cfu/
plate total aerobic mesophilic bacteria and 2.02.3 log
cfu/plate yeast and mold. Within the rooms, gutting

27

room air had the highest counts as 3.82 log cfu/plate.

Presence of these bacteria and yeast and mold in environmental air during processing may negatively inuence the total count on the product.
The water used in washing snails and cleaning has
been indicated to be microbiologically clean and drinkable (Tzouros & Arvanitoyannis, 2000). From this
point, we have analyzed the water used in the plant
and found the average aerobic mesophilic count as
1.30 log MPN/ml. No coliforms and E. coli were detected. These results indicate that the water used in the
plant did not pose microbiological risk for the process.
Results of this study indicated that raw material and
environmental air as the primary, and the personnel
hands and the equipment used as the secondary contamination sources among the control points examined in
the production steps of frozen snail meat. In addition,
the second boiling and freezing steps in snail meat production process had positive eects on the microbiological quality of the nal product, which can safely be
consumed.
Here we can conclude that rstly, frozen snail meat
processing plants should not approve the acceptance
of shelled snail with high initial microbial counts to
the plant. Secondly, plants should apply strict hygiene
and sanitary conditions during processing and storage
of the snail meat. Finally, we strongly recommend that
these kinds of plants must establish a HACCP based
program to produce a high-quality product safe for
consumption.

Acknowledgment
The authors would like to thank Aysegul Eyigor for
critical comments and revision for English.

References
Andrews, W. H. (1992). Manual of food quality control 4, Microbiological analysis (Rev. 1). Washington, DC: FAO Consultant, Food
and Drug Administration.
Andrews, W. H., & Hammack (2003). Salmonella. In L. A. Tomlison
(Ed.), Food and drug administration bacteriological analytical
manual. Hypertext Source: <http://www.cfsan.fda.gov/~ebam/
bam-5.html>.
Beliae, B., & Cochard, M. L. (1995). Applying geostatistics to
identication of spatial patterns of fecal contamination in a mussel
farming area (havre de la vanlee, France). Water Research, 29,
15411548.
Bojan, J. (2000). Essence of seafood HACCP of quality assurance.
Seafood Export Journal, 31, 4963.
Book of food material inspection and analyses procedures (1983).
General Publication (Vol. 65, pp. 604607). Ankara: Ministry of
Agriculture Foresty and Village Labor, Food Labor General Head
Oce.
Caklovica, F., Milanovic, A., Loncarevic, S., & Nedic, D. (1991). The
yield and quality of meat from snails (Helix pomatia), hedgehogs

28

S. Temelli et al. / Food Control 17 (2006) 2229

(Erinaceus europaeus) and turtles (Testudo graeca). VeterinariaSarajevo, 40, 6167.

Croci, L., Suredini, L., Cozzi, L., & Toti, L. (2002). Eects of
depuration of molluscs experimentally contaminated with Escherichia coli, Vibrio cholerae 01 and Vibrio parahaemolyticus. Journal
of Applied Microbiology, 92, 460465.
De Wit, J. C., & Kampelmacher, E. H. (1988). Some aspects of
bacterial contamination of hands of workers in food service
establishments. Zentralblatt fur Bakteriologie Mikrobiologie und
Hygiene B, 186, 4554.
Diliello, L. R. (1982). Methods in food and dairy microbiology.
Wesport: AVI Publishing Company.
Dore, W. J., Mackie, M., & Lees, D. N. (2003). Levels of male-specic
RNA bacteriophage and Escherichia coli in molluscan bivalve
shellsh from commercial harvesting areas. Letters in Applied
Microbiology, 36, 9296.
Dosdat, A., & de la Pomelie, C. (2000). Regulation and monitoring of
marine aquaculture in France. Journal of Applied Ichthyology, 16,
157162.
Drinking and potable water (1997). (TS 266). Ankara: Turkish
Standards Institute.
Ekanem, E. O., & Otti, B. N. (1997). Total plate count and coliform
levels in Nigerian periwinkles from fresh and brackish water. Food
Control, 8, 8789.
FAO (1998). The Codex general principles of food hygiene. Food
quality and safety systems. A training manual on food hygiene and
the Hazard Analysis and Critical Control Point (HACCP) system
(pp. 5560). Rome: Publishing Management Group, FAO Information Division.
Finley, J. W., Robinson, S. F., & Armstrong, D. J. (1992). Importance
of Hazard Analysis and Critical Control Point system in food
safety evaluation and planning. In D. A. Corlett (Ed.), Food safety
assessment (pp. 120130). Washington, DC: American Chemical
Society.
Formiga-Cruz, M., Allard, A. K., Conden-Hansson, A. C., Henshilwood, K., Hernroth, B. E., Jofre, J., et al. (2003). Evaluation of
potential indicators of viral contamination in shellsh and their
applicability to diverse geographical areas. Applied and Environmental Microbiology, 69, 15561563.
Fuchs, R. S., & Nicolaides, L. (1994). Incidence of Listeria in hot
and cold smoked sh. Letters in Applied Microbiology, 19, 394
396.
Geary, P. M., & Davies, C. M. (2003). Bacterial source tracking and
shellsh contamination in a coastal catchment. Water Science and
Technology, 47, 95100.
Giaccone, V., Ferri, M., & Colavita, G. (2002). Quantitative risk
assessment, methodological aspects. Rivista Di Coniglicoltura, 39,
2735.
Goulding, I. (2002). From catch the counter, keeping track of sh.
Seafood International, 17, 3336.
Graveland, J., & vanderWal, R. (1996). Decline in snail abundance due
to soil acidication causes eggshell defects in forest passerines.
Oecologia, 105, 351360.
Harrigan, W. F. (1998). Fish, shellsh and crustacea. Laboratory
methods in food microbiology (pp. 228233) (3rd ed.). London:
Academic Press Limited.
Harrigan, W. F., & McCance, M. E. (1976). Techniques in applied
microbiology. Laboratory methods in food and dairy microbiology
(pp. 141143). London: Academic Press Limited.
Hitchins, A. D. (2003). Detection and enumeration of Listeria
monocytogenes in foods. In L. A. Tomlison (Ed.). Food and drug
administration bacteriological analytical manual. Hypertext Source:
<http://www.cfsan.fda.gov/~ebam/bam-10.html>.
Huss, H. H. (1997). Control of indigenous pathogenic bacteria in
seafood. Food Control, 8, 9198.
Huss, H. H., Reilly, A., & Embarek, P. K. B. (2000). Prevention and
control of hazards in seafood. Food Control, 11, 149156.

ICMSF (1982). Microorganisms in foods. 1. Their signicance and

methods of enumeration (2nd ed., pp. 140143). Toronto: University
of Toronto Press.
Iida, T., Kanzaki, M., Nakama, A., Kokubo, Y., Maruyama, T., &
Kaneuchi, C. (1998). Detection of Listeria monocytogenes in
humans, animals and foods. Journal of Veterinary Medical Science,
60, 13411343.
ISO (1986). Dairy plant hygiene conditions general guidance on
inspection and sampling procedures (No: 8086). International
Organisation for Standardization Case Postale 56.Ch.1211, Geneva
20, Switzerland.
Ledergerber, S., Leadley, P. W., Stocklin, J., & Baur, B. (1998).
Feeding behavior of juvenile snails (Helix pomatia) to four plant
species grown at elevated atmospheric CO2. Acta Oecologica
International Journal of Ecology, 19, 8995.
Lipp, E. K., & Rose, J. B. (1997). The role of seafood in foodborne
diseases in the United States of America. Revue Scientique et
Technique De L Oce International Des Epizooties, 16, 620640.
Manual of seafood quality control (2000). Ankara: Ministry of
Agriculture Foresty and Village Labor, Prevention and Control
General Head Oce.
Mantovanelli, A., Marino, M., Comi, G., Vallavanti, W., & Dolzani,
L. (2001). Use of microbial analysis to test HACCP systems in food
industries. Industrie Alimentari, 40, 853865.
Marriott, N. G. (1999). Principles of food sanitation. Food contamination sources (4th ed., pp. 5359). Gaithersburg: Aspen Publishers,
Inc.
Martinez-Urtaza, J., Saco, M., Hernandez-Cordova, G., Lozano, A.,
Garcia-Martin, O., & Espinosa, J. (2003). Identication of Salmonella serovars isolated from live molluscan shellsh and their
signicance in the marine environment. Journal of Food Protection,
66, 226232.
Miossec, L., Guyader, F., Pelletier, D., Haugarreau, L., Caprais, M.
P., & Pommepuy, M. (2001). Le Validity of Escherichia coli,
enterovirus, and F-spesic RNA bacteriophages as indicators of
viral shellsh contamination. Journal of Shellsh Research, 20,
12231227.
Muniain-Mujika, I., Calvo, M., Lucena, F., & Girones, R. (2003).
Comparative analysis of viral pathogens and potential indicators in
shellsh. International Journal of Food Microbiology, 83, 7585.
Plusquellec, A., Beucher, M., Lelay, C., Gueguen, D., & Legal, Y.
(1994). Uptake and retention of Salmonella by bivalve shellsh.
Journal of Shellsh Research, 13, 221227.
Reed-Judkins, D. K., Farris, J. L., Cherry, D. S., & Cairns, J. (1998).
Foodborne uptake and sublethal eects of copper and zinc to
freshwater snails. Hydrobiologia, 364, 105118.
Romalde, J. L., Area, E., Sanchez, G., Ribao, C., Torrado, I., Abad,
X., et al. (2002). Prevalance of enterovirus and hepatitis A virus in
bivalve molluscs from Galicia (NW Spain): Inadequacy of the EU
standards of microbiological quality. International Journal of Food
Microbiology, 74, 119130.
SPSS Inc. (1992). SPSS for Windows, Release 6.0.
Steinhard, C. E., Doyle, M. E., & Cochrane, B. A. (1995). Foodborne
bacterial intoxications and infections. Food safety 1995, Foodborne
microbial illness (pp. 519521). Newyork: Marcel Dekker, Inc.
Swanson, K. M. J., Busta, F. F., Peterson, E. H., & Johnson, M. G.
(1992). Colony count methods. In C. Vanderzant & D. F.
Splittstoesser (Eds.), Compendium of methods for the microbiological examination of foods (pp. 7594). Washington, DC: American
Public Health Associations.
The oxoid manual (1998). (8th ed., p. 43, 280). Oxoid Ltd.: Hampshire,
England.
Tukel, C
, & Dogan, H. B. (2000). Staphylococcus aureus. Food
microbiology and their applications (2nd ed., pp. 357366).
Ankara: Sim Matbaaclk.
Tzouros, N. E., & Arvanitoyannis, I. S. (2000). Implementation of
Hazard Analysis Critical Control Point (HACCP) system to the

S. Temelli et al. / Food Control 17 (2006) 2229

sh/seafood industry: A review. Food Review International, 16,
273325.
nluturk, A., & Turantas, F. (1999). Food microbiology (pp. 110114).
U
_
Izmir:
Mengi Tan Basmevi.

29

Wittman, R. J., & Flick, G. J. (1995). Microbial contamination of

shellsh prevalence, risk to human health, and control strategies.
Annual Review of Public Health, 16, 123140.