Animal Feed Science and Technology 107 (2003) 161172

Changes in the levels of histamine during processing and storage of sh meal

Sevim Kse a, , Peter Quantick b , George Hall c
a

Department of Fisheries Technology, Faculty of Marine Sciences, Black Sea Technical University (Deniz Bilimleri Fakltesi, Karadeniz Teknik niversitesi), 61530 Camburnu, Trabzon, Turkey b University of Lincoln, Brayford Pool, Lincoln LN6 7TS, England, UK c Orchard House, Sea View, Ulverston, Cumbria LA12 7EX, England, UK Received 22 July 2002; received in revised form 27 March 2003; accepted 27 March 2003

Abstract Processing and storage trials were carried out under controlled laboratory conditions to investigate the effect of processing and storage conditions on histamine formation during sh meal production. It was found that most histamine concentrated in the press liquor (stickwater) meal after processing. Histamine levels were mainly decreased in mackerel samples but increased in cod samples after processing into sh meal. Histamine was detected in the sh meal samples of sh offal of both cod and mackerel. No bacterial growth was observed in the press-cake when sh was cooked and pressed during sh meal production. After drying of solids and the stickwater, bacterial growth was observed. This is an indication that sh meal is apparently microbiologically hygienic after cooking process, then recontamination occurs. That samples were packed in polyethylene bags seemed to show a slight increase in histamine levels up to fth week but a signicant decrease (P < 0.001) occurred gradually for the samples stored at 0, 20, 30 and 35 C. However, storage temperature did not have signicant effect on histamine levels for the packed samples. The results of storage trial with unpacked samples showed that histamine values decreased gradually with time at 15 C and 70% relative humidity (RH). Rapid loss and heavy mould growth occurred at 25 and 30 C with 80% RH. 2003 Elsevier Science B.V. All rights reserved.
Keywords: Histamine; Fish meal; Humidity effect; Temperature effect; Mould growth; Bacteria count

1. Introduction The presence of histamine in foods and feed stuffs at high levels is considered to be toxic and ingestion causes effects such as mortality, decreased weight gain and feed consumption
Corresponding author. Tel.: +90-462-7522805-5x120; fax: +90-462-7522158. E-mail addresses: sevimk@ktu.edu.tr, sevimkose@yahoo.com (S. Kse).

0377-8401/03/$ see front matter 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0377-8401(03)00127-5

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in chickens (Tapia-Salazar et al., 2001). The toxicity effect of histamine to chickens is called gizzard erosion (GE) or black vomiting due to the presence of black vomit in gizzards of affected chickens (Harry et al., 1975). Several researchers reported the role of sh meal and histamine on gizzard erosion in broilers (Janssen, 1971; Harry et al., 1975; Itakura et al., 1982; Taylor, 1986). The other amines such as putrescine and cadaverine which are elevated along with histamine in abused sh meal, were also known to induce clinical changes in gastric morphology of chickens and may potentiate the effects of histamine in vivo by inhibiting intestinal histamine-catabolizing enzymes (Taylor, 1986; Fairgrieve et al., 1994). In 1993, Japanese scientists isolated another GE-causing substance named as gizzerosine that was formed by the reaction of histamine or histidine and lysine during overheating of brown sh meal (Okazaki et al., 1983; Wagener et al., 1991). Although Bermudez and Firman (1998) and Friday et al. (1999) do not support the evidence of the effect of biogenic amines on gizzard erosion, several researchers previously reported and recently Barnes et al. (2001) proved that biogenic amines including histamine can cause gizzard erosion in broiler chickens. Barnes et al. (2001) conducted two studies to determine the effects of two common biogenic amines histamine (HIS) and cadaverine (CAD) on broilers growth and the incidence of pathologies associated with proventriculus. They found that histamine at 1 and 2 g/kg or the combination of HIS and CAD (1 g/kg each) reduced body weight and feed conversion at 21 days of age. HIS and CAD increased the total number, incidence and severity of gizzard erosion and proventriculus ulcers. Toxicity effects of sh meals containing histamine on a few other animals such as sh and shrimps were also studied (Fairgrieve et al., 1994; Opstvedt et al., 2000; Tapia-Salazar et al., 2001). Fairgrieve et al. (1994) carried out a feeding trial on rainbow trout supplementation with histamine alone (2 g/kg) or combined with putrescine and cadaverine (0.5 g/kg each). Although they found no depressing effect on the feed intake, growth or feed conversion and no signs of acute toxicity or mortality occurred in 16 weeks of study, they observed stomach distension syndrome. Fish meal is not only used in animal diet but is also used in human foods known as sh protein concentrate. Although it is not commonly reported, this type of meal can be a source of histamine poisoning in humans if high quality raw material and hygienic conditions are not applied during processing. Macan et al. (2000) observed histamine poisoning with people handling sh meal containing high histamine. They suggested that the lowest permissible levels of histamine in sh meal and similar products should be set and legally adopted. It was reported that histamine is used as a quality criterion for sh meals manufactured principally from warm water species such as anchovy, mackerel and sardine (Tapia-Salazar et al., 2001). Therefore, the presence of histamine in sh meal is still a common problem. Timetemperature effects have been thoroughly studied for histamine development in sh and other foods for human consumption (Edmunds and Eitenmiller, 1975; Hardy and Smith, 1976; Eitenmiller et al., 1987; Middlebrooks et al., 1988; Ababouch et al., 1991; Veciana-Nogus et al., 1997), however, there is little or no knowledge relating to histamine levels in sh meal stored under various storage conditions and the changes in the levels during sh meal production. Therefore, these areas were the subject of the current study.

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2. Materials and methods 2.1. Materials The sh used in the current study to process sh meal were mackerel (Scomber scombrus) and cod (Gadus callarias). All sh were provided as fresh from Grimsby Fish Docks, England. The actual sources of sh caught were unknown. The storage trials were carried out with commercial sh meal samples provided fresh from an English sh meal factory. The type of raw material used was industrial waste sh mainly 1:1 oily:white eshed sh. 2.2. Methods of analysis Histamine was analysed using the colorimetric method of Hardy and Smith (1976) modied by Kse and Hall (2000) for sh meal or bony sh samples. The equilibrium relative humidity (aw ) was measured using a Novasina water activity meter. Readings were taken at 25 0.1 C every 30 min by which time equilibrium had been attained. The sellotape technique was used to examine and identify moulds in the samples during storage trials. Firstly, a sellotape strip (about 45 cm long) was pressed onto the colony. The strip was then pressed onto a clean microscope slide with a drop of Lactophenol Cotton Blue. Observation and identication were carried out according to the method of Onions et al. (1981). A parallel study was carried out with pure cultures of the common species for comparison. The procedure by Ward and Morgan (1991) was used for analysis of aatoxins. Total viable count (TVC) and coliform count were carried out according to the Food and Drug Administration (1978) and Collins et al. (1989). The method of Yoshinaga and Frank (1982) was used for histamine forming bacteria count (HFB). Standard Plate Count Agar was used for TVC, modied Nivens medium for HFB (Niven et al., 1981; Yoshinaga and Frank, 1982), and Violet Red Bile Glucose Agar for coliform count. Api 20E (Api, LA Balme Les Grottes, France) test kits were used for biochemical tests for microbial identications. Statistical analysis was carried out according to Sokal and Roh (1987). 2.3. Experimental trials 2.3.1. Effect of processing Two different trials were carried out to test the changes in histamine levels during sh meal processing. Fish meal was produced under laboratory conditions. Firstly, if large sized sh were used, they were cut into small pieces. They were cooked in boiling water in a steam pan for 2025 min stirring occasionally and cooled for 10 min without stirring. After cooling, the surface water was drawn off. The esh and bones were packed into muslin bags by pressing for approximately 5 min in a screw press. The resulting liquor is called stickwater. Any particles of sh in the press liquor were screened out and returned to the press cake. The press cake was spread out thinly onto trays, placed under an air dryer (45 C) and turned repeatedly to prevent scorching. The dried product was ground using a knife mill. The process was carried out by adjusting neness, starting from 1 cm to 1 mm hole diameters. In order to remove oil from the stickwater, the liquor was stored between 0

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and 4 C for few days to form a gel-type solid with the oil concentrated on top and easily separated. The stickwater was concentrated to one-tenth of its original volume in a climbing lm evaporator (operating temperature: 80 C and vacuum pressure: 24 inches mercury) before freeze drying. 2.3.2. First trial Eight kilogram of fresh mackerel from the same batch was rstly divided into two groups. One of the groups was lleted to make a third group. The whole sh, the llets and lleting waste were stored at room temperature on trays for 42 h, then processed separately into sh meal under laboratory conditions using the method mentioned earlier. Sampling was carried out by taking different parts of the sh from each groups and homogenised in a mixer (holding capacity: 11 l and mixing capacity: 4.5 l). Histamine and moisture content analyses were carried out just before processing, after cooking and after processing. The freeze drying procedure for drying stickwater was used to produce stickwater meal. 2.3.3. Second trial The sh meal was produced from 1-day-old mackerel (originally stored in the open air at room temperature, 20 C). Then, the same procedure was carried out as in the rst trial except that raw materials and the yield products were weighed at each stage of processing in order to be able to calculate the total amount of histamine formed for nal results. Cod sh was also used as a control for this experiment because it was reported that cod contains low histidine levels while mackerel contains high histidine levels (Lukton and Olcott, 1958). The calculation of histamine level at each stage of processing was carried out by taking into account of any losses which occurred as well as the varying moisture content at each stage where losses occur. The oil in the product for the second and third trial was not removed during processing in order to prevent miscalculation in the weight losses that would have affected the calculation of histamine. TVC, HFB and coliform counts were carried out for each stage of both mackerel and cod meal productions. 2.3.4. Storage trials Two storage trials were carried out to study time, temperature and humidity effects on the histamine formation and the presence in commercial sh meal. 2.3.5. First trial with sh meal packed in polyethylene bags Ten kilogram of commercial sh meal samples were divided into four groups. Each group was packed in a polyethylene bag and stored at 0, 20, 30 and 40 C for up to 14 weeks. Histamine (mg/100 g), water activity (aw ), and moisture content (g/kg) were determined at the beginning of each week for up to sixth week excluding fourth week, then at the beginning of 13th and 14th week. Relative humidity (RH) was not measured after samples were initially packed. 2.3.6. Second storage trial with the sh meal samples without packing This trial was conducted with four series according to the temperature and humidity applied. Each series proceeded with samples stored in controlled relative humidity cabinets without packaging. Sampling was carried out weekly and each sample was analysed for

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histamine, moisture content and aw . Series 1 and 2 were stored at 30 C and 80% RH. Series 3 was stored at 25 C and 80% RH. Series 4 was stored at 15 C and 70% RH.

3. Results and discussion Table 1 shows the results of the rst processing trial. The majority of histamine was found in the mackerel esh meal rather than in offal meal (guts, heads and bones, etc.). Histamine was mainly concentrated in the stickwater meal for all samples. Since histamine is water soluble, it is natural that histamine will be extracted from raw sh during processing (cooking and pressing) into press water and not destroyed by further processing (freeze drying). Fig. 1 represents the results of the second processing trial that was carried out with mackerel to study the effect of processing on histamine formation. There was high loss (168.79 mg/100 g) in histamine level after total raw sh was processed. Although the histamine level (mg/100 g and in the total weight) in the stickwater meal was higher than llet meal itself, the difference was far lower than the difference between offal meal and its stickwater meal. This observation may be due to either high histamine levels or high bacterial load (histamine-forming bacteria) in the guts, gills, etc. of the sh. These results are important since the potential for histamine formation will be higher if sh meal is produced from industrial waste sh which contains a high amount of guts, gills or heads. Compared to the results of the rst trial, histamine levels were higher for sh llets and meals originating from the llets than the samples of sh offal and offal meals. Arnold and Brown (1978) reported that histamine and other biogenic amines can be broken down by several microorganisms. They also reported that a strain of Proteus (now Morganella) morganii produced large amounts of histamine after being inoculated into a sterile tuna esh homogenate. However, a signicant amount of histamine was soon decomposed by the same organism. Therefore, the above differences may be explained as histamine breakdown to other compounds. Ienistea (1971) reported that histamine is heat-resistant to a certain degree. In tuna sh, it is partially destroyed by boiling at 102 C for 3 h and sterilisation for 90 min at 116 C in small cans results in its total destruction. Therefore, the overall loss (dry weight base (DWB)) in histamine level after processing could be explained as a processing loss by product sticking to the equipment used, or breakdown to other compounds. It was reported that more histamine was produced in the red muscle sh such as mackerel species than in
Table 1 The results of rst trial showing concentration of histamine (mg/100 g DWB) at the various stages of sh meal production Sampling Histamine (mg/100 g DWB) Fish llet Raw sh After cooking & pressing After processing Stickwater meal 103.85 (3.07) 89.66 (4.25) 80.42 (2.73) 368.72 (11.77) Fish offal 79.61 (4.06) 29.98 (7.30) 16.73 (1.25) 127.93 (5.71) Whole mackerel 96.03 (3.50) 63.62 (4.03) 61.06 (1.50) 415.24 (6.05)

Figures represent the means of three determinations. S.D. are given in parentheses.

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Fig. 1. The results for processing effect on histamine formation for mackerel meal. (All the results were calculated as DWB, as triplicated (or more). The weight used for sampling and loss due to handling and processing was also taken into account for calculations. Parentheses represent the calculated amount of histamine in total batch used for experiment. Stickwater.)

white muscle. Cod is known to be white muscled sh (Arnold and Brown, 1978). Lukton and Olcott (1958) reported that cod contained low histidine levels and mackerel contained high histidine levels. The results of the second processing trial carried out with cod (Fig. 2) showed that although no histamine was expected to be found in cod or cod meal, some was detected, but only in guts and gills (1.39 mg/100 g wet weight base (WWB) histamine). This was calculated as 7.03 mg/100 g as dry weight base (DWB) for the whole unprocessed (raw) cod before processing. After processing, there was still no histamine in the cod meal dried from

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Fig. 2. The results for processing effect on histamine formation for cod meal. (All the results were calculated as DWB, as triplicated (or more). The weight used for sampling and loss due to handling and processing was also taken into account for calculations. Parentheses represent the calculated amount of histamine in total batch used for experiment.)

pressed solid, but 83.40 mg/100 g of histamine (DWB) was found in the dried stickwater meal of cod, which was expected to originate from offal since the pressing and cooking can cause extraction of histamine into stickwater. The gain in histamine level in total weight was calculated as 10.13 mg/100 g which is greater than a 100% increase at the end of processing. One of the reasons for the increase might be due to histamine formation in the stickwater which was stored for a short time at room temperature. It is interesting to note that majority of histamine was removed into stickwater as was also observed in the mackerel samples.

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Table 2 The changes of TVC, HFB and coliform counts (log cfu/g) during sh meal production from cod and mackerel batches of second trial Samples processing stages Fresh After 1 day stored at room temperature Solids after cooking Solids after drying & milling Stickwater after drying Mackerel TVC 3.89 (0.12) 5.94 (0.06)
a

Cod HFB 3.71 (0.21) 5.85 (0.11)

a

Coliform 2.81 (0.09) 5.25 (0.01)

a

TVC 3.88 (0.12) 6.30 (0.07)

a

HFB 2.43 (0.10) 6.24 (0.14)

a

Coliform 2.24 (0.03) 5.76 (0.11)

a

2.90 (0.16) 4.70 (0.14)

2.60 (0.12) 4.29 (0.08)

2.02 (0.03) 3.16 (0.02)

4.11 (0.12) 4.60 (0.21)

4.04 (0.09) 4.04 (0.06)

3.65 (0.09) 3.13 (0.09)

Results represent means of three determinations. Figures in parentheses represent S.D. a >30 cfu/g (log 1.4 cfu/g).

These results point out that using stickwater meal for feeding animals can be more toxic compared to meals produced from the sh solids and care must be taken when using it. Table 2 shows initial microbial conditions of the samples used for the second processing trial and the microbial changes during sh meal production. Total viable count (TVC), histamine-forming bacteria (HFB) and coliform count increased during storing of sh in open air at room temperature. When sh was cooked and pressed, no bacterial growth was observed in the press-cake. After drying of solids and the stickwater, bacterial growth was observed. This is an indication that sh meal is apparently free of microorganisms (microbiological hygienic) after cooking process. Some damaged cells may recover later (DAoust, 1981). However, recontamination occurred during drying, milling and handling mainly from environment and equipment after cooking. Highest recontamination was observed in the stickwater meal. The change in bacterial count during processing stages were signicant (P < 0.001) for both mackerel and cod meal (in the second processing effect trial). The common histamine forming bacteria identied in sh meal were Morganella morganii, Providencia rettgeri, Escherichia coli, Klebsiella oxytoco and Klebsiella pneumoniae. These bacteria are reported as common histamine producers, especially M. morganii (Taylor et al., 1978; Behling and Taylor, 1982; Taylor, 1986; Rodriguez-Jerez et al., 1993). M. morganii was also reported as histamine decomposer (Arnold and Brown, 1978). Table 3 shows the histamine results of the rst storage trial with varying temperatures depend on time. There were no signicant differences in water activity results throughout the trial. The aw results of the samples stored at 0, 20, 30, 35 C were 0.51, 0.51, 0.49 and 0.44, respectively. The moisture content results also did not vary much during the rst trial at 0 and 20 C but there was a slight fall from 92.6 to 83.0 g/kg at 30 C and a rapid decrease from 92.6 to 57.0 g/kg at 35 C which was to be expected due to evaporation at higher temperatures, the loss of water vapour from the bag being exacerbated by the action of sampling. Except for samples stored at 35 C, there was an apparent initial increase in histamine level up to week 5 and a decrease noted after that as being signicant for all the temperatures (P < 0.001). The increase in histamine level was negligible for the samples stored at 35 C, but 27.5% decrease occurred at the 14th week compared to the rst day of

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Table 3 Changes in histamine levels during rst storage trial for sh meal samples which were packed in polyethylene bags and stored at different temperatures Temperature ( C) 0 20 30 35 Histamine levels (mg/100 g DWB) in weeks 0 126.6 (7.1) 126.8 (7.1) 126.8 (7.1) 126.8 (7.1) 1 126.3 (7.9) 120.8 (6.7) 120.4 (3.4) 124.0 (2.6) 2 128.9 (11.8) 125.9 (7.0) 118.0 (3.1) 120.8 (8.9) 3 129.1 (3.7) 126.3 (1.6) 121.1 (7.1) 125.4 (4.9) 5 134.1 (7.8) 138.2 (5.5) 133.0 (6.1) 125.3 (6.9) 8 124.6 (1.7) 117.7 (1.3) 110.4 (2.6) 120.5 (2.4) 13 110.4 (5.9) 114.3 (4.5) 107.0 (5.5) 116.5 (2.3) 14 100.9 (1.5) 96.5 (1.2) 95.3 (2.3) 91.9 (3.2)

Results represent means for three determinations. Figures in parentheses represent S.D. Statistical analysis was explained in the text.

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Table 4 The results of second storage trial of unpacked samples at different humidity and temperature conditions Storage condition 30 C; 80% RH Series 1 Weeks 0a 2 3 30 C; 80% RH 2 0 2 3 0 1 2 3 4 0 1 2 3 4 68 Histamine mg/100 g DWB 1.51 (0.04) 1.26 (0.01) Heavy mould growth 2.55 (0.0) 0.12 (0.0) Heavy mould growth 57.79 (5.51) 59.16 (7.29) 56.76 (2.23) 4.98 (0.42) Heavy mould growth 80.96 (2.01) 67.08 (2.03) 60.18 (2.85) 58.69 (5.66) 57.62 (0.94) No mould growth aw 0.29 (0.03) 0.89 (0.01) 0.33 (0.02) 0.84 (0.01) 0.39 (0.01) 0.78 (0.03) 0.86 (0.03) 0.84 (0.02) 0.34 (0.01) 0.65 (0.003) 0.56 (0.004) 0.55 (0.003) 0.55 (0.0) Moisture content (%) 5.10 (0.05) 10.76 (0.06) 5.15 (0.04) 14.48 (0.05) 5.72 (0.04) 15.70 (0.06) 19.69 (0.05) 19.07 (0.99) 5.00 (0.01) 9.73 (0.02) 9.00 (0.04) 8.94 (0.03) 8.90 (0.02)

25 C; 80% RH

15 C; 70% RH

Data in parentheses represent S.D. of three determinations. Statistical analysis was explained in the text. a Initial values.

the storage. Storage temperature did not have a signicant effect on histamine values for the samples packed. The second storage trial (Table 4) was carried out for the same aim as in the rst trial except that the samples were not packed but were left open under controlled relative humidity conditions. Therefore, the effect of %RH was also tested. The changes in the values of histamine, aw , and moisture content were found to be signicant with Series 1 and 2 (P < 0.001). There was a rapid loss in histamine level and a heavy mould growth observation with Series 1 and 2 at the beginning of the third week. There was no signicant change in histamine levels up to the second week with Series 3, then a signicant fall (P < 0.001) occurred followed by heavy mould growth. Signicant changes were found in the values of both aw and moisture up to the second week. No mould growth was observed with Series 4 which was stored at 15 C and 70% RH. The change in aw levels and moisture contents were signicant (P < 0.001) up to the second and third weeks, respectively. However, the change in histamine level was only found signicant (P < 0.001) for the rst week. The results show that histamine levels decrease gradually with time at lower temperatures and humidity, but rapid loss can occur with high temperatures and humidity. The absence of mould growth at 15 C and 70% RH may be explained as aw playing a limiting factor for mould growth at these conditions. Some moulds were identied to genus level as Penicillium and Aspergillus spp. The samples were analysed for possible aatoxin presence. According to the results, there was no aatoxin present in four mouldy and 16 non-mouldy sh samples. However, more tests and further investigation are required for a conclusive decision on whether aatoxin or other mycotoxins could form in the sh meal as they are reported to occur in mixed animal feeds (Morgan et al., 1986; Morgan and Lee, 1990).

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4. Conclusion The study provides new information on the effect of processing and storage conditions on histamine levels in sh meal, which has not been available previously. Using stickwater meal (meal made from press liquor) is not advisable since it is possible that it contains high histamine levels unless produced from fresh raw material. Histamine levels were quite stable under anaerobic conditions for extended periods. Fish meal is hygroscopic leading to mould growth under aerobic conditions. Therefore, without using polyethylene bags, it was also discovered that mould growth occurred at high humidity and temperatures with resulting rapid decrease in histamine levels. The decline in histamine levels in earlier stages is most likely to be attributable to early mould growth. However, mould growth is unacceptable in sh meal unless it is conducted in a controlled environment with appropriate microbes. Testing sh meal for histamine content is a common safety action for poultry and sh farmers. Using low temperatures and humidity for storing sh meal samples will prevent histamine development and mould growth. However, the preferred means of control is in raw materials for sh meal. The results of this study will be benecial to both sh meal producers and farmers. References
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