Available Online: http://www.ejpau.media.pl/volume17/issue4/art-04.html
RELATIONSHIP BETWEEN MICROBIAL LOAD AND HISTAMINE CONTENT IN THE RAINBOW TROUT FILLET DURING REFRIGERATION
Mohammad Hassan Kamani1, Omid Safari2, Seyed Ali Mortazavi3, Sahar Sabahi4, Masoomeh Mehraban Sang Atash5
1 Young Researchers and Elite Club, Sabzevar Branch, Islamic Azad University, Sabzevar, Iran
2 Department of Fishery, Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad, Mashhad, Iran
3 Department of Food Science and Technology, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
4 Department of Food Science and Technology, Sabzevar Branch, Islamic Azad University, Sabzevar, Iran
5 Food Science and Technology Research Institute, ACECR Mashhad Branch, Mashhad, Iran
The aim of the present study was to evaluate the relationship
between histamine content and microbial load of refrigerated rainbow trout fillet
during different storage times (0, 5, 10, 15 and 20 days). In order to determine
the extent of reduction in quality of the fillets, spoilage indicators including
total bacterial load, psychrotropic bacteria, coliforms, Lactobacillus,
staphilococci, yeast and mold, E. coli and Salmonella were studied.
The results showed that histamine content increased significantly (p < 0.05)
from 1.96 to 7.98 mg kg-1 during 20-day storage. The bacterial load
of the plates indicated that all bacterial spoilage parameters with the exception
significantly during the 20-day refrigeration period, in which the highest rate
of growth was achieved for the psychrotropic bacteria (10.23 log CFU g-1)
and total bacterial load (11.48 log CFU g-1). All fillets were declared
unfit for consumption after the fifth day of preservation according to the allowable
limit defined for the total bacterial load (7 log CFU g-1). No salmonella and E.
coli were observed in all samples. There was a highly significantly (p < 0.01)
positive correlation (0.64) between histamine content and total bacterial load.
Generally, the results indicated that total bacterial load and psychrotropic
bacteria were more beneficial than histamine content to determine the reduction
of fillet quality. It was found that histamine could not be regarded as a suitable
spoilage parameter in trout as its level failed to achieve the European Community
Standard of 100 mg kg-1. The histamine increase rate was on the other
hand highly dependent upon the total bacterial load, coliforms, yeast and molds,
all of them can result from the rise in the content of this parameter during
the spoilage process.
The aim of the present study was to evaluate the relationship between histamine content and microbial load of refrigerated rainbow trout fillet during different storage times (0, 5, 10, 15 and 20 days). In order to determine the extent of reduction in quality of the fillets, spoilage indicators including total bacterial load, psychrotropic bacteria, coliforms, Lactobacillus, staphilococci, yeast and mold, E. coli and Salmonella were studied. The results showed that histamine content increased significantly (p < 0.05) from 1.96 to 7.98 mg kg-1 during 20-day storage. The bacterial load of the plates indicated that all bacterial spoilage parameters with the exception staphilococci increased significantly during the 20-day refrigeration period, in which the highest rate of growth was achieved for the psychrotropic bacteria (10.23 log CFU g-1) and total bacterial load (11.48 log CFU g-1). All fillets were declared unfit for consumption after the fifth day of preservation according to the allowable limit defined for the total bacterial load (7 log CFU g-1). No salmonella and E. coli were observed in all samples. There was a highly significantly (p < 0.01) positive correlation (0.64) between histamine content and total bacterial load. Generally, the results indicated that total bacterial load and psychrotropic bacteria were more beneficial than histamine content to determine the reduction of fillet quality. It was found that histamine could not be regarded as a suitable spoilage parameter in trout as its level failed to achieve the European Community Standard of 100 mg kg-1. The histamine increase rate was on the other hand highly dependent upon the total bacterial load, coliforms, yeast and molds, all of them can result from the rise in the content of this parameter during the spoilage process.
Key words: Rainbow trout, fillet, storage time, quality parameters.
The most important commodities traded in value terms are shrimp (15%), salmon and trout (14%), ground fish (9%, e.g. hake, cod, haddock and Alaska pollock) and tuna (8%), respectively . About 85%, or 132.3 million tonnes, of total fishery production is used for direct human consumption and 46% of the fish destined for human consumption is in live and fresh form [5, 17]. Among the seafood products, the rainbow trout is one of nutritive products with globally extensive culture in aquaculture industry and considerable marketability in the household food basket. Nowadays, the ability to supply fresh aquatic food has gained enormous importance . The rainbow trout is mainly supplied as covered in ice and does not have a very long shelf-life. Many factors affect the shelf-life of the rainbow trout but bacterial growth is considered to be the most important . Gelatine - chitosan composite in the rainbow trout  and sodium acetate and nisin in the grass carp  are some of the solutions presented concerning the changes in the quality of the fish during cold preservation and problems resulting from their bacterial growth.
Growth and activity of microorganisms lead to disintegrations which in turn cause fish to spoil. This spoilage results in the production of metabolites in the meat that cause off-odour and off-taste . The form and extent of the micro-organisms in the fish is dependent upon many factors which include their habitat (fresh water or sea water, the water temperature, pelagic or benthic and the water pollution level), post-fishing transportation and preservation manner (preservation by freezing, preservation in ice, preservation with refrigeration) and handling. Pseudomonas, Moraxella, Acinobacter, Shewanella, Flavobacterium, and Vibriones containing Vibrio and Photobacterium, and Aeromonas are among the gram-negative psychrophilic bacteria which are predominant in fish. Also, there are gram-positive bacteria such as Bacillus, Micrococcus, Clostridium and Lactobacillus as deteriorating agents of flesh quality. Entrobacteriaceae is prevalent in the polluted water while Esherichia coli and Salmonella can survive for long periods in warm water .
Another group of microorganisms are involved in the decarboxylation of meat, which is mainly done by Entrobacteriaceae, Pseudomonas, Micrococcus and lactic bacteria families that lead to the production of biogenic amines. Biogenic amines are organic alkali with low molecular weight produced by the bacterial decarboxylation of free amino acids by decarboxylus acid enzyme following the removal of alpha carboxyls. Histamine which is produced by the bacterial decarboxylation of histidine is one of the most important amines which cause histamine poisoning in the consumer, especially when it is present in high levels [23, 24]. Regarding the increasing culture of the rainbow trout and the time necessary to transport the fish from the farms to the stores, the quality control of fish freshness from the viewpoints of chemically and bacterially and the relationships between them are becoming more essential. Therefore, the aim of the present study was to evaluate the microbiological and chemical criteria in rainbow trout fillet and determination of relationship between microbial load and histamine content in the rainbow trout fillet during refrigeration.
MATERIALS AND METHODS
Freshly caught rainbow trout with an average weight of 600 ± 50 g were purchased from a farm on the outskirts of Mashhad (Khorasan Razavi Province, Iran) and immediately transported to the ACECR laboratory covered in ice.Then, the fish was filleted, placed in separately coded packages and refrigerated for 0, 5, 10, 15 and 20 days at 4 ± 1ºC. The fillets were removed from the refrigerator on the designated days and subjected to biochemical and bacterial tests.
Measurment of Histamine Content
The histamine in the rainbow trout fillet was extracted by placing the fillets in trichloroacetic acid (5%) and then isolated by adding benzyl chloride. The extent of the histamine in the fillets was then measured by adding isocratic methanol and water in a 62:38 ratio in the opposite direction to the flow of the solvent. The histamine content was determined with comparison of the peak preservation times of the unknown sample with that of the standard sample via referring to the standard graph and measuring the area below the peak curves .
A sample was taken from the anterior-dorsal area of each fillet. Thereafter, 10 g of each sample was transferred to the Stomacher bags under sterile conditions and 90 g of Ringer’s Solution was then added. The bag was placed in the Stomacher machine and homogenization was performed for 10 min. The final sample with a dilution level of 0.1 was used to prepare subsequent dilution levels. The total bacterial load was measured using Kant Agar Culture Plates (ACP, Merk) which were incubated at 30ºC for 24 to 48 hours. Similar medium was also used to enumerate psychrophilic bacteria at 7ºC for 10 hours. The enumeration of the coliforms was performed in violet and red bile agar culture mediums where the plates were incubated for 1 hour at 37ºC . The lactic acid bacteria were enumerated in the deMan, Rogosa, and Sharpe (MRS) culture media and the plates were incubated in an anaerobic jar at 30ºC for 2 to 3 days . Yeast and mould were enumerated in the potato dextrose agar (PDA) medium and incubated at 25ºC for 3 to 5 days . The Staphylococcus was enumerated in Baird Parker culture medium containing egg yolk and potassium tellurite following incubation at 37ºC for 2 days . The data were presented as the natural log while the total enumerations were given in log CFU/g ± SD. Esherichia coli was identified using the EC broth, Lauryl sulphate tryptose broth, and LST broth culture media. Confirmation tests were performed on fume-producing samples in eosine methylene blue agar (EMBA) culture medium and the IMViC test was also conducted. To detect Salmonella, 10 g of the sample was homogenized with 90 ml lactose broth and incubated at 35°C for pre-enrichment. Selective enrichment was performed in tetrathionate broth at 43°C for 24 hr and selenite cystine broth at 35°C for 24 hr followed by plating on Salmonella-Shigella (SS) agar and brilliant-green phenol-red lactose sucrose (BG) agar incubated at 35°C for 24 hr. Suspected colonies developed on each plate were used to biochemical and serological analysis .
One-way ANOVA and the post-hoc Tukey’s test were performed using the statistical software SPSS 18 in order to show significant differences between treatments (p < 0.05) The tests were performed using completely randomized design (CRD) at three replicates. The regressive relationship between histamine contents during the time intervals was analysed with XLSTAT 12. The Pearson's correlation test was also performed to investigate the correlation among the parameters under analysis (p < 0.05).
The changes in histamine content during the preservation period at 4ºC are shown in Table 1. The results indicated a rising trend in histamine content during the 20-day preservation period, which was considered to be statistically significant (p < 0.05). The lowest amount of histamine was measured at 1.96 mg kg-1 on the first day and no significant rise was observed until the tenth day. The rising trend became statistically significant thereafter until it reached its highest value of 7.98 mg kg-1 on day 20 (p < 0.05). The regression relationship between histamine content during preservation time resulted in the following equation.
Histamine content [mg kg-1] = 1.95 – 0.25 DAY + 0.03 DAY2 (r2adjusted = 0.891) (1)
Table 1. The mean ( ± SD1) of histamine content and total bacterial load and counts [log CFU g-1] of psychrophilic bacteria, coliforms, Lactobacillus bacteria, staphylococci, yeast and mold, Escherichia coli, and Salmonella in the refrigerated rainbow trout fillet during 20 days2
1 Standard deviation
2 Different superscripts (a–d) within rows indicate significant differences at p > 0.05
3 Not determined
Total Bacterial Load
As shown in Table 1, there was a significant rising trend in bacterial load in the rainbow trout fillet during storage time (p < 0.05). The initial number of the total bacterial load was 3.29 log CFU g-1 which significantly (p < 0.05) increased throughout the preservation period with the exception of days 10 to 15. The highest number counted on day 20 showed an increase of 8.19 to 11.48 log CFU g-1 (p < 0.05). There was a significant (p < 0.01) positive correlation (r = 0.642) between total bacterial load and histamine content (Tab. 2).
Table 2.Correlation coefficients (R) between histamine content [mg kg-1]and microbial counts [log CFU g-1]
* Correlation is significant at 0.05 level
** Correlation is significant at 0.01 level
The initial number of psychrophilic bacteria in fresh fillet was 3.14 log CFU g-1 that showed a significant rising trend (p < 0.05) during the entire preservation period (Tab. 1). The rate of increase was higher in the first ten days than those of second one. The final number measured on day 20 was 10.23 log CFU g-1 (p < 0.05). There was a significant (p < 0.05) positive correlation (r = 0.580) between psychrophilic bacteria and histamine content (Tab. 2).
The results of analysis the coliform count in the rainbow trout fillet are given in Table 1. The results indicated a significant rising trend in colifom counts in the rainbow trout fillet during the preservation period (p < 0.05). The initial number of coliform bacteria was 2.67 log CFU g-1, which increased significantly (p < 0.05) throughout the preservation period with the exception of days 10 to 15. The highest number counted on day 20 showed an increase from 6.47 to 9.14 log CFU g-1. There was a highly significant (p < 0.01) positive correlation (r = 0.721) between coliform and histamine content (Tab. 2).
No bacteria were observed in the fresh fillet (Tab. 1). However, there was a significant rising trend in Lactobacillus count in the rainbow trout fillet during the preservation period (p < 0.05). The highest Lactobacillus count (5.29 log CFU g-1) was observed on day 20. The rate of increase was higher during the first ten days than that of the last one. The least changes were observed between 10 and 15 day of preservation. There was a significant (p < 0.05) positive correlation (r = 0.591) between Lactobacillus count and histamine content (Tab. 2).
The initial number of Staphylococcus bacteria was 1.29 log CFU g-1, that increased significantly (p < 0.05) throughout the preservation period and reached its highest value on day 20 (5.02 log CFU g-1) (Tab. 1). There was a significant (p < 0.05) positive correlation (r = 0.545) between Staphylococcus count and histamine content (Tab. 2).
Yeast and Mold
There were no yeast and mold in the fresh fillet (Tab. 1). However, the yeast and mold counts significantly (p < 0.05) rose during the entire preservation period. The final number measured on the day 20 was 9.83 log CFU g-1 (p < 0.05). The rate of increase was higher during the first ten days than that of the last one. No significant changes in the yeast and mold count were observed between 10 and 15 day of preservation (p > 0.05).
Esherichia coli and Salmonella
Neither Esherichia coli nor Salmonella were observed in the fresh and the refrigerated fillets throughout time periods.
Histamine as a non-volatile organic alkaline compound with small molecular weight is one of the most important biogenic amines. The spoilage of fish fillet and the increase in bacterial load lead to the creation of a group of bacteria containing the histidine decarboxylase enzyme which can be used to determine the level of spoilage in fish fillet . A rising increase in histamine content in the rainbow trout fillet was observed throughout the preservation period. This pattern can be attributed to the protease activity of endogenous enzymes due to the rise in the bacterial load . The histidine decarboxylase reacts with histidine in the muscles and thus leads to the gradual increase in the level of histamine in fish following fishing.
The histological potential and decarboxylase activity of histamine is explained by the presence of certain bacteria groups which mainly consist of mesophilicenterobacteria and are highly active at ambient temperature . As mezophiles are the bacteria that produce histamine and cold preservation cannot guarantee the survival of Mesophilic bacteria, it is necessary to enquire how histamine is produced during refrigeration. The reason lies in the fact that some of the histamine-producing bacteria such as psychrophilic and lactic acid are very tolerant to media temperature restrictions and so their ability to produce histamine in ice or even when frozen remains unaffected albeit in smaller quantities. In the present study the rising trend observed in histamine corresponded to a similar trend in both psychrophilic and lactic acid bacteria which is a confirmation of this fact. Histamine and other biogenic amines are heat resistant chemical parameters of spoilage which do not easily disintegrate. Therefore, they can be used to assess the quality of these amines even in food heated for human consumption. Lactobacillus breuis, Lactobacillus buchnerii, Lactobacillus curuatus and Lactobacillus carnis are examples of the most important lactic acid bacteria that produces biogenic amines . Different values have been reported for initial quantity of histamine in rainbow trout fillet . This difference can be attributed to various factors such as the initial concentration of the histidine, the rate of bacterial growth and activity, storage conditions, and temperature [18, 26].
The histamine produced in foodstuffs causes histamine poisoning which produces effects such as itching, flushing and nausea . The European Commission has declared 100 mg kg-1 as the highest allowable quantity of histamine in fish, while the United States Food and Drug Administration has lowered this to 50 mg kg-1 . No sample under investigation in this study reached this limit. Investigations in this study indicated a suitable non-linear relationship between the quantity of histamine and refrigeration time, which can be used to estimate the quantity of histamine in the rainbow trout fillet. The histamine measurements in this research are in consistent with the results of other research in the rainbow trout fish . The amount of histamine in the control rainbow trout fillet preserved and significant correlation between histamine and bacterial parameters show that our results are also in consistent with findings in other research [13, 21].
Total Bacterial Load
Bacterial growth is the main cause of spoilage in foodstuffs, which when developed leads to the production of off-odour and off-favour and the subsequent rejection of the foodstuff by consumer. The ever-present gram-negative Entrobacteriaceae, the bacteria that produce H2S, and the lactic acid bacteria are the most important causes of spoilage and in particular off-odour. Although, the initial bacterial load the in freshwater fish is different and dependent on the condition of water and fishery temperature, a high quantity load can be found on the raw product which can be attributed to the storage conditions and manipulation . The results indicated a statistically significant rising trend in the quantity of all parameters in the rainbow trout with the exception of staphylococci. In the present study, the initial total bacterial load for all parameters was less than 4 log CFU g-1 which is an indicator of good quality of the fish . The actual figure was in fact 3.29 log CFU g-1 which rose to a final value of 11.48 log CFU g-1 indicating the complete spoilage of the fish. The standard value for the total bacterial load is 7 log CFU g-1  that was attained in the fish in this study on day 5 with no noticeable increase during the next 10 days. This growth model was similar to the growth model in salmon in a fifteen-day preservation period  and farmed rainbow trout in a 20-day preservation period both in ice . Different time periods to reach the total bacterial load in fish have been reported. The total bacterial load in the rainbow trout fillet refrigerated for 12 days and the sea bass refrigerated for 7 days exceeded 7 log CFU g-1 .
Gram-negative psychrophilic bacteria are among the principal and dominant bacterial groups in meat which greatly aid the spoilage of meat preserved in cold aerobic conditions . The rate of this increase was higher at the beginning of the preservation period and the highest rate of increase was observed during the first ten days with the rate slowing subsequently. The growth rate for psychrophilic bacteria is higher than that of other microorganisms because of the favourable environment. The initial quantity and growth rate of these bacteria are extremely dependent on the total bacterial load and the preservation environment so that it had exceeded the allowable limit in the refrigerated rainbow trout fillet on the twentieth day . The quantity of psychrophilic bacteria in the refrigerated rainbow trout fillet increased from 3.85 to 8.43 log CFU g-1 during a 16-day refrigeration period which was in consistent with other study . These bacteria were found to have the highest correlation coefficient with the coliform bacteria which indicates a positively significant relationship. The maximum allowable limit for psychrophilic bacteria in the rainbow trout fillet is 7 log CFU g-1  and according to this standard, the fish preserved in this research were fit for consumption until the fifth or sixth day.
The quantity of coliforms showed a rising trend during the preservation period. The rate of this increase was higher at the beginning of the period so that the highest rate of increase was observed in the first 10 days and then it slowed down. The coliform growth model in the fillets was in consistent with that of meagre fish . The quantity of coliforms in the fillets is dependent upon important factors such as fishery environment, fishing conditions and handling. For instance, the initial and final quantity of the coliforms in the rainbow trout fillet when it was frozen for five months was reported to be zero .
The quantity of lactic acid bacteria is as vital as other psychrophilic bacteria in assessment of the fish quality . The Lactobacillus count showed a rising trend during the preservation period. The rate of this increase was higher at the beginning of the period meaning that the highest rate of increase was observed in the first 10 days. This increase in the logarithmic growth can be the result of the appropriate growing environment due to the fall in the quantity of pH resulted from production of lactic acid by anaerobic glycolysis of the fish during the early period of preservation. The bacterial growth rate slowed after the tenth day to the extent that the rate of increase during the 10th to the 15th day of preservation was not statistically significant. The lactic acid bacteria are among the optional anaerobic group of bacteria which are gram-positive and have the ability to grow in environments with relatively low pH value. Some of these bacteria can cause the catabolism of amino acids via deamination or decarboxylation and lead to the production of carbon dioxide, ammonia and volatile fatty acids. Arginine is the most common of these metabolised amino acids which its decarboxylation can produce biogenic amino toxins and sulphur-containing amino acids which can subsequently lead to an increase in the production of H2S in the tissue. The rising trend in lactic acid bacteria in the refrigerated rainbow trout fillet was in consistent with the results of other research .
In the present study, the quantity of the staphylococci did not show any significant rising trend during the preservation period. This group of micro-organisms was the least correlated group with the quantity of histamine and other bacterial groups. The growth of the staphylococci is improved in the salty foods and foods that do not involve much water activity which could explain their lack significant growth in freshwater media. The low quantity of these bacteria in fish fillet does not cause problems. However, a very large quantity could lead to food poisoning. Staphylococcus aureus is the most important species in bacterial spoilage in this regard. The allowable limit for this bacterial group and especially the Staphylococcus aureus species is therefore recommended to be 3 log CFU g-1 .
Yeast and Mold Count
Yeast and mold form another micro-organismic group which cause the fish to spoil and are visible in large coloured or uncoloured colonies . Most molds can use pectin, fats, proteins and organic acids as a substrate for their growth. According to the results, the quantity of yeast and mold in the rainbow trout fillet showed a similar rising pattern to the other bacterial parameters. The quantity of yeast and mold did not increase in the early days of preservation despite a reduction in pH value, which indicates their resistance to low pH values. These micro-organisms can continue their activity at low temperatures and low water activity. The increase in yeast and mold can cause adverse changes in the sensory properties of food such as taste, odour, and colour . In research carried out on cold-smoked salmon preserved at 8ºC, the quantity of yeast and mold increased from 1.5 to 3.5 log CFU g-1 . However, in another research on frozen rainbow trout, this group was not detected until the 3rd month, which is indicative of the role of freezing on the quantity of yeast and mold .
Esherichia coli and Salmonella Count
Fish ponds can be easily polluted by human waste and surface water and should be controlled in outbreak of intestinal bacterial infection. The results indicated that none of the rainbow trout fillets contained Escherichia coli or Salmonella, which are similar to the results for Escherichia coli in fish cubes  and Salmonella in frozen rainbow trout . However, both Escherichia coli and Salmonella were observed in bacterial investigation of fresh Alosa kessleri . Salmonella has been recognized as the main cause of gastroenteritis in Germany for over a century. Escherichia coli is also considered as a pathogen that causes bloody diarrhoea, chronic kidney failure, haemolytic uremic syndrome . Pond water, fishing technique, handling method, filleting, laboratory cleanliness and packaging can be indicative of the existence of these microorganisms .
This study investigated the relationship between histamine content and microbial load (total bacterial load and counts of psychrophilic bacteria, coliforms, Lactobacillus, staphylococci, yeast and mold, Escherichia coli and Salmonella) during a 20-day refrigeration period. The results indicated the highest correlation coefficient between histamine and coliforms. Also, total bacterial load and psychrotropic bacteria were more useful than histamine content to determine the reduction of fillet quality. The results of these analyses showed optimal quality for rainbow trout fillets stored under these conditions, and established a microbiological shelf-life of 5 days.
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Accepted for print: 16.10.2014
Mohammad Hassan Kamani
Young Researchers and Elite Club, Sabzevar Branch, Islamic Azad University, Sabzevar, Iran
Islamic Azad University of Sabzevar
Sabzevar, Khorasan Razavi Province
P.O. Box 9618814711
Phone: +98 938 1669927
Fax: +98 571 2647513
Department of Fishery, Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad, Mashhad, Iran
Tel: +98 5138805466
Fax: +98 5138788805
Cell Phone: +98 9103005738
Seyed Ali Mortazavi
Department of Food Science and Technology, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
Department of Food Science and Technology, Sabzevar Branch, Islamic Azad University, Sabzevar, Iran
Masoomeh Mehraban Sang Atash
Food Science and Technology Research Institute, ACECR Mashhad Branch, Mashhad, Iran
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