Bacteriological study of cultured silver carp
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Iranian Journal of Fisheries Sciences 12(3) 689- 701 2013 __________________________________________________________________________________________ Bacteriological study of cultured silver carp (Hypophthalmichthys molitrix) in Gilan province, Iran Razavilar V.; Khani M. R.*; Motallebi A. A. Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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… __________________________________________________________________________________________ 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; Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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 __________________________________________________________________________________ 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. Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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… __________________________________________________________________________________________ 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 Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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 __________________________________________________________________________________ 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… __________________________________________________________________________________________ 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 Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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 __________________________________________________________________________________ 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. Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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… __________________________________________________________________________________________ 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 Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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 __________________________________________________________________________________ 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 Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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… __________________________________________________________________________________________ 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 Downloaded from jifro.ir at 9:12 +0430 on Tuesday May 19th 2020 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
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