Bacteriological study of cultured silver carp

 
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 (p
690 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. This
692 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 then
Iranian 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 (p
694 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 P
Iranian 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 × 104
698 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 higher
Iranian 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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