Bacteriological study of cultured silver carp
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Iranian Journal of Fisheries Sciences 12(3) 689- 701 2013
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Bacteriological study of cultured silver carp
(Hypophthalmichthys molitrix) in Gilan province, Iran
Razavilar V.; Khani M. R.*; Motallebi A. A.
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Received: January 2012 Accepted: April 2012
Abstract
The study was undertaken to determine bacterial contamination of warm-water fish ponds
and silver carps harvested from those ponds in Guilan province, Iran. In this respect, water
samples were taken from 7 ponds and investigated by testing total bacteria, coliforms, and
Escherichia coli. In addition, skin swab samples of silver carps caught from each pond were
studied for enumeration of the same bacteria as well as Staphylococcus aureus and also for
the presence of some human bacterial pathogens including Salmonella spp., Vibrio spp., and
Listeria monocytogenes. For all bacteriological examination techniques of International
Organization for Standardization were followed. Results showed that mean water bacterial
quality in ponds was significantly different (p690 Razavilar et al., Bacteriological study of cultured silver carp…
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Introduction other factors which influence the quality
Fish are considered as safe, nutritious and and safety of the fish (Jayasinghe and
beneficial food. However, aquaculture Rajakaruna, 2005; Reynisson et al., 2009;
yields can be associated with certain food CAC, 2010; FDA, 2011). Microbial
safety issues (WHO, 2007). The quality of farmed fish is largely
importance of aquaculture continues to determined by the quality of the water in
expand, especially for freshwater species. which they were cultivated (Buras, 1993;
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Based on FAO (2012), almost one third of Ekpo et al., 2010). The edible muscle
fish used for human consumption are tissue of finfish is normally sterile at the
produced in aquaculture. Increasing time of capture and bacteria are usually
demand for fish and seafood has had an present on the skin, gills and in the
increase trend in recent years with annual intestinal tract (CAC, 2010). However,
growth rate of 8.5%. This trend is likely to some bacteria such as Staphylococcus spp.
be continued, with the contribution of may be found only in the body surface
aquaculture to fish food supply estimated (Ekpo et al., 2010). The microbial count in
to reach 60% by 2020 (Washington and different fishes have showed that the
Ababouch, 2011). number of organisms were more on the
One of the essential things in food body surface of big fishes with higher
hygiene is the examination of food, body weight than on the surface of small
especially for the presence of fishes, because the organisms use the
microorganisms. This is very much needed surface area of the fish as a microhabitat in
for the protection and maintenance of their ecosystem (ibid.). After fish is being
community health (Sujatha et al., 2011). caught and dying, the immune system
Fish are often infected with or may harbor collapses and bacteria are allowed to
various bacteria which may cause health proliferate freely on the skin surface
hazards to the fisherman, fish handlers and (Emikpe et al., 2011). However, the type
even to the consumers (Monzur-Hassan et of microorganism found associated with a
al., 1994). Several studies have particular fish depends on the water it was
demonstrated many bacteria species found. Freshly harvested aquaculture
encountered in different fish which are products, particularly those from tropical
potentially pathogenic (Feldhusen, 2000; regions, may harbor pathogenic bacteria
Razavilar, 2002; Phong Lan et al., 2007; which form part of natural micro-flora of
Ekpo et al., 2010; Sujatha et al., 2011). fish ponds (Claucas and Ward, 1996).
The level of bacterial Thus, water and fish quality are very
contamination in fish at the time of capture important subjects to protect public health
and the nature of the pathogenic bacteria in with a special emphasis on the
fish depends on many factors such as the microbiology.
bacteriological quality of the harvest Human pathogens have been
water, natural conditions when fish is reported to be associated with different
captured, handling practices and some types of fish (Abou-Elela and Farag,Iranian Journal of Fisheries Sciences, 12(3), 2013 691
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2004). The fish that live in water polluted north of Iran through the harvesting season
with human and the animal fecal matter in winter. The ponds were located in four
may carry considerable numbers of main regions. The water resource of ponds
bacteria such as Salmonella, V. cholera, E. was mainly supplied by Sefidrood River,
coli and other Coliforms (Jayasinghe and except for A and B ponds which were
Rajakaruna, 2005). Human infections and mainly supplied by underground waters.
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intoxications caused by pathogens Four species of warm-water fish including
transmitted from fish are quite common common carp (Cyprinus carpio), silver
and the following bacteria have been carp (Hypophthalmichthys molitrix),
recorded: Salmonella spp., Escherichia bighead carp (H. nobilis), and grass carp
coli, Vibrio parahaemolyticus, Vibrio (Ctenopharyngodon idella) were cultured
cholerae, Staphylococcus aureus and in those ponds from which only silver carp
Listeria monocytogenes (Novotny et al., was considered in this study.
2004). Outbreaks usually occur due to the In the first step, water in fish ponds
consumption of raw or insufficiently heat- was aimed to investigate. Water samples
treated fish, which may be contaminated were then collected from three sites of
with bacteria from water environment each pond (inlet, middle, and outlet) from
(Vibrio spp.) or terrestrial sources about 10 to 30 cm below the surface with
(Salmonella spp., Staphylococcus spp., V. separate sterile plastic containers and then
cholerae) (Novotny et al., 2004). In the were pooled as a representative sample.
case of poor hygiene, the contamination of Another representative sample was taken
fish and fish products may increase due to in the same way, so that we had two
unsanitary procedures, the rotation of the samples from each pond for bacterial
assigned duties of workers (ibid.). examinations. The water temperature of
Carp species such as silver carp are fish ponds ranged from 8 – 12oC and pH
one of the most important economical and from 7.3 – 8.1. After collection, the water
widely cultivated warm water fish in Iran samples were sent to the laboratory within
which is widely sold and used in its fresh 12 h. They were kept at 4 – 5oC during the
(Salehi, 2006, 2009). The aim of this study transfer and examined within 24 h of
was to investigate some bacterial sampling. In the laboratory, each sample
contamination of water in warm-water fish was first blended with vortex apparatus for
ponds and silver carps cultivated in those 10 seconds. Then for enumerating total
ponds in Guilan province, Iran. bacteria, coliforms, and E. coli, serial
decimal dilution of the water sample was
Materials and methods prepared by adding 1 ml of sample in
The study was carried out in seven warm- sterile test tube, containing 9 ml of sterile
water fish ponds (named from A to G) peptone water solution and this 1-in-10
which were randomly selected from dilution was then homogenized with
different localities of Guilan province, vortex apparatus for 10 seconds. This692 Razavilar et al., Bacteriological study of cultured silver carp…
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dilution was then used for bacteriological blended with vortex apparatus for 10
analyses directly or diluted further in the seconds and serial decimal dilution was
same way. The bacteriological techniques made of each fish swab sample using the
of the International Organization for peptone water diluents. Then
Standardization (ISO) including ISO 4833 bacteriological examinations was
(2003), ISO 4832 (2006), and ISO 7251 performed to enumerate total bacteria,
(2005) were used for enumeration of total coliforms, E.coli, and Staphylococcus
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bacteria at 25 °C, coliforms at 30 °C, and aureus and to detect the presence of
E. coli at 44 °C, respectively. Results Salmonella spp., Vibrio cholera, Vibrio
expressed in counts of cell-forming units parahaemolyticus, and Listeria
(CFU) per ml of fish ponds’ water. monocytogenes. In this respect, swab
In the next step, silver carps which samples were cultured on general and
were captured from the studied ponds were selective media for enumeration and
sampled through the harvesting season, detection of studied bacteria by using the
before being sent to the market. In this ISO bacteriological techniques (ISO 4833:
respect, at the same time which the water 2003, ISO 4832: 2006, ISO 7251: 2005,
samples were collected, six silver carps ISO 6888-1: 1999, ISO 6579: 2002,
were randomly collected immediately after ISO/TS 21872-1: 2007, and ISO 11290-2:
they had been harvested from each warm- 1998), within 24 h of sampling. The
water fish pond. Those chosen for this isolates were identified by series of
study had average length from 45 to 50 cm biochemical and physiological tests
and average weight from 2 to 2.5 kg. according to the related ISO procedure for
Samples from skin of silver carps were that bacterium. For examination of total
taken by sterile cotton tipped swab from bacteria and coliforms, the related plates
each fish from external surface using the were aerobically incubated at 25 °C and 30
methods described by American Public °C, respectively. Results expressed in
Health Association (APHA) (Nickelson et counts of CFU per cm2 of fish skin or
al., 2001). Skin samples were taken from a detection of bacteria per surface area of
50 cm2 central area of the fish by marking sampling.
out, using a sterile template. Swab It is worth mentioning that all the
sampling were conducted as soon as used materials during water sampling of
possible after the fish were caught, then fish ponds and swab sampling of silver
the swabs were placed and shaken each in carps were sterile or had been sterilized
tubes containing 5 ml of Phosphate buffer before sampling processes. Media used for
saline (Pbs), separately and sent to detection and confirmatory tests, were
laboratories for bacteriological purchased from Merck, and prepared
examinations. The swab samples were according to the manufacturer’s
transported to the laboratory within 12 h instructions.
and were kept at 4 – 5°C during the All of the results are presented as
transfer. There, each sample was first mean values. One-way ANOVA was thenIranian Journal of Fisheries Sciences, 12(3), 2013 693
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applied to statistically analyze data, and if significantly lower values than other ponds
there was a significant difference (p694 Razavilar et al., Bacteriological study of cultured silver carp…
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Table 1: Means of bacterial counts (cfu/ml) obtained from water samples of seven studied ponds
Ponds Total bacteria Coliform bacteria E. coli
A 1.36×103 *e 2.50×101 *f -
B 9.10×102 *g 1.20×101 *g -
C 7.21×103 *c 2.86×102 *d -
D 1.86×104 *b 8.37×102 *b 2.5×101 *c
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E 3.42×104 *a 1.03×103 *a 4.2×101 *a
F 1.21×103 *f 4.60×101 *e -
G 5.92×103 *d 3.88×102 *c 3.2×101 *b
*
Means within a column, which are not preceded by a common superscript letter(s) are significantly
different according to Duncan Multiple Range Test at PIranian Journal of Fisheries Sciences, 12(3), 2013 695
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Discussion to more contaminate than underground
This paper describes a study where resource. For instance, water fowls like
different bacteria were tested to evaluate Geese and Swans that live around rivers,
the bacterial load of warm-water fish as Doyle and Ericson (2006) declared, can
ponds and contamination of silver carps be a significant source of bacteria that
which captured from these ponds. elevate bacteria counts.
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In our study, a comparison of In this study, no E. coli detected in
reference bacterial counts (total bacteria the analyzed water samples of ponds when
and coliforms) in pond water samples with their coliform counts were lower than 2.86
the data provided by other authors × 102 cfu/ml, and this bacterium was only
(Ntengwe and Edema, 2008; Macedo et detected from those ponds with counts
al., 2011) is indicative of low above 3.88 × 102 cfu/ml. Also there was a
contamination of the ponds. When the positive correlation among the higher
bacterial counts in water are low, these coliform counts and higher E. coli counts.
microorganisms will be present in skin In regards to the isolation of coliforms
mucus and the digestive tract, but not in such as E. coli in some fish ponds, which
muscle tissue (El-Shafai et al., 2004). TBC is an indicator of fecal contamination
in pond water samples were in the range of (Feldhusen, 2000; Ekpo et al., 2010),
9.1 × 102 – 3.42 × 104 cfu/ml which were results are in accordance with those
lower than values recorded by Ntengwe obtained by Doyle and Ericson (2006) who
and Edema (2008) in the order of 106 reported that the ponds that harbor the fish
cfu/ml with the temperature of the ponds could be the source of contaminates due to
ranged from 17 to 25 °C. The obtained indiscriminate deposition of human,
lower counts may be related to the lower animal excreta and other environmental
temperature of the studied ponds which wastes into them. In addition to the
ranged from 8 to 12 oC. Also coliform potential risks of E. coli in fish skin for
counts were lower than that recorded by human consumption, being eaten raw or
Macedo et al. (2011) who recorded 9.4 × undercooked, the presence of E. coli in
103 – 3× 108 coliforms MPN/100ml in the pond water can also put human beings at
rainy period. risk if they caught fish from the ponds and
Ponds A and B contained did not wash their hands before eating
significantly lower values of coliforms and anything (Ntengwe and Edema, 2008).
total bacteria in compared to other ponds. Average of total bacterial counts of
This could be related to the water resource fish swab samples in studied ponds were
of these ponds which were mainly supplied ranged from 1.89 × 104 to 8.23 × 104
by underground waters. However, other cfu/cm2. These are in accordance with
ponds supplied by Sefidrood River those reported by Zmysłowska et al.
introduced higher bacterial counts which (2002) that skin mucus usually contains
could be due to the exposure of this source 102 – 107 bacteria per cm2 of skin.696 Razavilar et al., Bacteriological study of cultured silver carp…
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Moreover, these values was found to be may accompany handling fresh fish or
markedly lower than the recommended consumption of improperly cooked fish.
public health and safety standard value of The considerably high counts of
between 106 – 107, approved by Institute of coliforms and detecting E. coli recorded in
Standards and Industrial Research of Iran this study indicates relative fecal
(ISIRI). For fresh fish, the microbiological contamination of fish which could be
limit for human consumption proposed by related to fecal contamination of studied
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the International Commission on fish ponds’ water. This is in accordance
Microbiological Specifications for Foods with those obtained by Monzur-Hassan et
(ICMSF) (1986) is 5 × 105 to 107 cfu/cm2 al. (1994) who related presence of E. coli
in aerobic plate count analysis, which is in fish to the fecal contamination of water
also in line with our results. with warm blooded animals. Also
About 90% of the fish swab unhygienic handling of fish introduces the
samples investigated during the present E. coli as secondary bacterial contaminates
study contained the coliform counts (ibid.).
>102/cm2 with a potential of causing health Despite the lower values of
hazards as stated in study conducted by coliforms and total bacteria obtained in
Jayasinghe and Rajakaruna (2005). water samples of ponds B and A, these
However, most of the samples (57%) did values in fish swab samples collected from
not contain E. coli while 43% of 42 those ponds were higher than other ponds,
investigated samples of fish were with relatively. This is in disagreement with the
counts more than 2 and less than 6 per report of Ekpo et al. (2010), who
cm2. This is in disagreement with the suggested a strong relationship exist
report of Sivakami et al. (2008) who between fish bacterial load and that of the
worked on microbial species in carps and water ecosystem. This difference could be
noted that 50% of the organisms in carps due to the unfavorable effect of the
were E. coli and Pseudomonas aeruginosa. harvesting conditions on the bacterial
According to ICMSF (1986) that contamination of fish. Therefore,
recommended an ‘m’ value of 11 E. coli precaution should be taken to prevent
per cm2 of fresh fish, results came in this water contamination during harvesting as
study revealed that the quality of silver well as post harvest handling of fish
carps harvested from fish ponds is (Emikpe et al., 2011). The microbial load
satisfactory. The contamination of food of of fish can also be improved through
fish origin with pathogenic E. coli regular disinfection of catching gears or
probably occurs during handling of fish working equipment, and brief immersion
and during the production process of caught fishes in disinfecting solution
(Novotny et al., 2004). Thus, as Empike et such as brine water to reduce the microbial
al. (2011) suggests, the public should be load on the fish before storing at cold
enlightened on the inherent danger that temperature or sold to the public (ibid.).Iranian Journal of Fisheries Sciences, 12(3), 2013 697
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Nevertheless, the bacteriological results of infected fish in S. aureus counts and the
other ponds did not show this kind of isolation of pathogenic bacteria. This is
difference. Furthermore, water samples of again in accordance with the findings of
pond E showed highest bacterial counts, other researchers (Abou-Elela and Farag,
and also fish samples of this pond revealed 2004; El-Shafai et al., 2004; Harnisz and
highest counts of E. coli and S. aureus and Tucholski, 2010) who noticed that the
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detection of some pathogenic bacteria, microbiological quality of fishes is directly
compared to other ponds. This suggests related to the quality of the water in which
there is a relationship between bacterial they are cultivated and harvested.
contamination in fish and bacteriological Fish bacteriological results pointed
quality of the harvest water which is in out that E. coli counts had a positive
accordance with those obtained by other correlation with S. aureus counts. This is
researchers (Jayasinghe and Rajakaruna, in disagreement with report of Novotny et
2005; Reynisson et al. 2009; Ekpo et al., al. (2004) who declared such organism
2010). Besides, the co-existence of E. coli should not be present on fresh-caught fish.
and the gram-positive S. aureus which The presence of this fecal indicator
cause food poisoning could have been bacterium in the fish could also be
transferred through contact with skin of correlated with the presence of other
handlers (Eze et al., 2011). pathogens. However, we did not find
Significant differences were correlation between the values of
observed among the total bacterial counts coliforms and E. coli and isolation of
and coliform counts in the fish harvested V.cholera and L. monocytogenes. Similar
from the seven ponds. This difference to this finding, some authors (Feldhusen,
could be due to the bacteriological quality 2000; Abou-Elela and Farag, 2004) have
of the water in which fish are harvested reported that no correlation was found
(CAC, 2010). However, silver carps between the presence of fecal coliforms
harvested from the least contaminated and some pathogens e.g. Vibrio spp. In
pond (pond B) were the most infected fish regards to Feldhusen (2000) and Novotny
in total bacteria, coliforms, and E. coli et al. (2004) reports, these isolated
counts; but lower counts of S. aureus and pathogens could be considered as potential
pathogenic bacteria were observed in this food safety hazards of aquaculture
pond. This finding is similar to those products. Also silver carp could be
reported by Harnisz and Tucholski (2010) considered as potential sources of infection
who noticed that the percentage content of with L. monocytogenes such as rainbow
aerobic and facultative bacteria decreased trout (Oncorhynchus mykiss) and salmon
with an increase in total microbial counts. (Salmo salar) which have been focused on
Moreover, our results showed that silver during recent years (Novotny et al., 2004).
carps harvested from more contaminated The fish harvested from pond D
ponds (Ponds E, D, and G) were the most with total bacterial count of 1.89 × 104698 Razavilar et al., Bacteriological study of cultured silver carp…
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cfu/cm2 which was the lowest count temperatures in other seasons, which might
compared to the other ponds produced cause the detection of more bacteria in
V.cholera and L. monocytogenes, while ponds and fishes, could not be considered.
ponds A and B which had the highest TBC Similar relationships were obtained by
in fish did not produce these pathogens. Zmysłowska et al. (2002); Jayasinghe and
These pathogens which categorized in Rajakaruna (2005) who noticed that the
indigenous bacteria group, when present in lowest counts of the microorganisms
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fresh cultured products, are usually found determined were usually attained in winter,
at fairly low levels, and where these while higher counts were recorded in
products are adequately cooked, food autumn and spring or in higher
safety hazards are insignificant temperature zones. This observation can be
(Feldhusen, 2000). However, these related not only to the lower water
microorganisms could also enter seafood temperature in winter, but also to the fact
processing chain because of inadequate that silver carp primarily feed in the water
process control, poor standards of hygiene column where bacterial concentrations are
and sanitation in processing plants and lower (Phong Lan et al., 2007).
post-production contamination during Silver carps were found to harbor a
incorrect handling or storage (Claucas and number of pathogenic microorganisms in
Ward, 1996). varying percentages on their skin.
Also results revealed that, none of However, the quality of silver carps
the samples investigated contained harvested from warm-water fish ponds in
Salmonella spp. and V. parahaemolyticus. Guilan province, north of Iran were
This could indicate that the fish harvested satisfactory in some bacterial indices, but
in the Guilan Province were free from detection of E. coli, V. cholera, and L.
these highly pathogenic bacteria. monocytogenes from fish samples could be
Salmonella can be present both in water, considered as potential food safety hazards
especially of contaminated ponds, and in and initiate various fish-borne diseases in
the fresh fish from these areas, but low human if fish prepared improperly. The
incidence and even absence is not bacteriological qualities of these fishes
uncommon (Feldhusen, 2000). could be substantially worse after
Many factors influence the unhygienic fish handling, cleaning and
microflora of finfish, the most important purchase in the local retail markets than
ones being water temperature, proximity of that at harvest. Thus, it is recommended
harvesting areas to human habitations, that a thorough surveillance of the
quantity and origin of food consumed by microbiological status of fish be done for
fish, and method of harvesting (CAC, the safety of the ultimate consumers.
2010). Since the period of the investigation Moreover, there is need for the Iranian fish
was in the cold season (winter) and the farms and industry to improve on their fish
water temperature in the ponds was low farming management, such as, fish food
(ranged 8 – 12oC), the effect of higherIranian Journal of Fisheries Sciences, 12(3), 2013 699
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preparation, environmental sanitation and fecal-contaminated ponds.
monitoring for quality fish yield. Environmental Research, 95, 231-
238.
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