HISTAMINE AND HISTAMINE-FORMING BACTERIA IN KEROPOK LEKOR

Download Histamine and Histamine-Forming Bacteria in Keropok lekor (Malaysian Fish Sausage) during Processing. Mahmud Ab Rashid NOR-KHAIZURA. 1*, Ha...
0 downloads 627 Views 785KB Size
Download PDF
Love PNG Images
Food Sci. Technol. Res., 15 (4), 395 – 402, 2009

Histamine and Histamine-Forming Bacteria in Keropok lekor (Malaysian Fish Sausage) during Processing Mahmud Ab Rashid nor-khaizura1*, Hassan zaiton2, Bakar jamiLah3, Rahmat Ali Gulam ruSuL4 and Mohammad Rashedi iSmaiL-FitrY3 1

Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia

2

Faculty of Science and Technology, Islamic Science University of Malaysia, 71800 Nilai, Negeri Sembilan, Malaysia Department of Food Technology, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 Serdang, Selangor,

3

Malaysia 4

School of Industrial Technology, Universiti Sains Malaysia, 11800 Minden, Penang, Malaysia

Received November 27, 2008; Accepted March 24, 2009 Keropok lekor at different processing stages were obtained and examined for total volatile bases (TVB), trimethylamine (TMA), putrescine, cadaverine and histamine and their forming bacteria. TVB and TMA levels decreased significantly (p < 0.05) after boiling from 7.29 to 4.68 mg/ 100g and 3.38 to 1.81 mg/ 100g, respectively. After cooling stage, the levels of TMA, putrescine, cadaverine and histamine in keropok lekor were increased significantly (p < 0.05). Putrescine, cadaverine and histamine level for all samples was found less than allowable level, which is 50 ppm. Bacteria forming putrescine, cadaverine and histamine reduced significantly (p < 0.05) after boiling stage and it was increased significantly (p < 0.05) after cooling stage. Before the boiling stage, microorganisms isolated producing putrescine, cadaverine and histamine were members of the family Enterobacteriaceae and also members of Staphylococcus, Pseudomonas and Micrococcus genera. Members of the genera Pseudomonas that produce biogenic amines were not found from keropok lekor after the boiling stage. Keywords: Histamine, Histamine-forming bacteria, keropok lekor

Introduction Keropok lekor is a popular and highly relished fish product in Malaysia. Keropok lekor normally prepared with a mixture of fish to starch at 1:1 ratio, added with salt, sugar and monosodium glutamate (msg). The processing of keropok lekor involves mainly five stages comprises of mincing the fish meat, mixing the minced fish with other ingredients, kneading the dough, boiling and cooling before it is packaged. At present, most of manufacturers producing keropok lekor carry out the processing manually with little mechanization. This product can be easily found in night market, hawkers stall and also most of the school canteen. Keropok lekor are served as appetizer or snack with local special chilli sauce. In fish products, a number of spoilage indicators have *To whom correspondence should be addressed. E-mail: [email protected]

been used; these include total volatile bases (TVB), trimethylamine (TMA) and biogenic amines (Botta et al., 1984a, 1984b; Hebard et al., 1982; Mietz and Karmas, 1978). TVB and TMA are widely used to determine fish product quality. Analysis for TVB involves the estimation of all volatile amines produce during spoilage. Meanwhile, TMA are resulted from the reduction of trimethylamine-oxide (TMAO) by bacterial activity and intrinsic enzymes. It is often used as an index of freshness of fish and fish products (Hush 1988; Villareal and Pozo, 1990). The levels of TVB and TMA that have been considered as the upper limit in fishery products are 30 – 35 mg/ 100 g (Hush, 1988; Sikorski et al., 1989; Connell, 1995) and 10 – 15 mg/ 100 g (Sikorski et al., 1989; Connell, 1995). While, biogenic amines especially histamine, putrescine and cadaverine, have been suggested as indicators of spoilage for some foods, such as fresh fish, meat and vegetables (Riebroy et al., 2004). The importance of estimating the concentration of biogenic amines in fish and fish products

396

is related to their impact on human health and food quality. To the present, information on chemical quality of keropok lekor is very limited. Most studies carried out previously on keropok lekor were focus on the physical characteristics of the final product (Siaw et al., 1985; Kyaw et al., 1999; Cheow, 1998; Yu, 1992), and on the processing and formulation of keropok lekor (Sidaway and Balasingam, 1971; Siaw et al., 1979; Yu et al., 1981). The objective of the study was to determine levels of total volatile bases (TVB), trimethylamine (TMA), putrescine, cadaverine and histamine and their forming bacteria at different stages of keropok lekor processing (kneading, boiling and cooling stage). Materials and Methods Sample collection Five hundred grams samples were collected at different processing stages for 5 replications. The processing stages are after kneading the dough, after boiling and after cooling stage. The kneading process was done manually at ambient temperature. Furthermore, the boiling process was carried out in the boiler at 100℃ for 10 min and cooling process was done at room temperature, where boiled keropok lekor was arranged on the stainless steel table and allowed to cool for about 1 to 2 h. Samples were obtained using sterile utensils and were placed into sterile plastic bags, which were properly labelled and dated. Samples were brought to the laboratory in a pre-chilled container with crushed ice (4 ± 1℃) and analysed within 24 h. Determination of Total Volatile Bases (TVB) and Trimethylamine (TMA) Total volatile bases (TVB) and trimethylamine (TMA) were determined using Conway’s Microdiffusion Method (Ng and Low, 1992). Sample preparation Two grams of sample were weighed on aluminium foil and transferred into a mortar and grinded. 8mL of 4% Trichloroacetic acid (TCA) (Fisher Chemicals) was added and grinded. The mixture was allowed to stand for 30 min at ambient temperature and grinded occasionally. The mixture was than centrifuged (Kubota, 2100) at 3000 rpm for 10 min. The filtrate was kept at -20℃ in a freezer before proceeding to the next step. Total Volatile Bases (TVB) Sealing agent was applied to Conway’s unit. 1 mL of inner ring solution (Appendix C) was pipette into inner ring. Then, 1 mL of sample solution was pipette into outer ring. The Conway’s unit with cover was slanted and 1 mL of saturated Potassium carbonate solution (K2CO3) (Ajax Chemicals) was pipette into the outer ring. The Conway’s unit was immediately closed and tightened with clip. The outer ring solution was mixed gently and allowed to stand for 60 min at 37℃ in an incubator (Binder, BD 53). After incubation, the inner ring solution was titrated against 0.02N Hydrochloric acid (Fisher Scientific) using a

m. a. r. nor-khaizura et al.

micro-burette unit, until the green color turns pink. Blank test was carried out using 1 mL of 4% TCA instead of sample solution (Conway and Byrne, 1933). Trimetylamine (TMA) Sealing agent was applied to Conway’s unit. 1 mL of inner ring solution was pipette into inner ring. Then, 1 mL of sample solution was pipette into outer ring. 1 mL of neutralized 10% formaldehyde (R&M Chemicals) was pipette into the outer ring and the outer ring solutions were gently mixed. The Conway’s unit with cover was slanted and 1 mL of saturated K2CO3 solution (Ajax Chemicals) was pipette into the outer ring. The Conway’s unit was immediately closed and tightened with clip. The outer ring solution was mixed gently and allowed to stand for 60 min at 37℃ in an incubator. The inner ring solution was titrated against 0.02N Hydrochloric acid (Fisher Scientific) using a micro-burette unit, until the green color turned pink. Blank test was carried out using 1 mL of 4% TCA instead sample solution (Conway and Byrne, 1933). Biogenic amines analysis The samples were ground in a Waring blender for 3 min. 5 g sample was transferred to a 50 mL centrifuge tube and homogenized with 20 mL of 6% trichloroacetic acid (TCA) for 3 min. The homogenate was centrifuged at 8000 × g, for 10 min at 4℃ and filtered through Whatman No. 2 filter paper. The filtrate was placed in a volumetric flask and made up to 50 mL. Samples of standard biogenic amine solutions and 2 mL aliquots of the sample extracts were derivatized with benzoyl chloride according to the previously described method (Hwang et al., 1997). The benzoyl derivatives were dissolved in 1 mL of methanol and 20 μl aliquots were used for high-performance liquid chromatography (HPLC) injection. Amines were determined by using HPLC (Shimadzu, Japan, consisting of a Model LC-6A pump, Model SPD-6A UV detector set at 254 nm, a Model C-R6A chromatopac integrator). A LiChrosopher 100RP – 18 reverse phase column (5 μm, 125 × 4 mm I.D., E.Merck) was used for the separation. The gradient elution program was set at 0.8 mL/min, started with a methanol-water mixture (50:50, v/v) for 0.5 min. The program proceeded linearly to methanol-water (85:15, v/v), with a flow rate of 0.8 mL/min over 6.5 min. This was followed by the same composition and flow rate for 5 min, then a decreased over 2 min to methanol-water (50:50, v/v) at 0.8 mL/min. Isolation of histamine- forming bacteria Twenty five grams of keropok lekor at each processing stages was aseptically transferred to a sterile stomacher bag and pummelled for 1 min in a stomacher (Seaward Stomacher 400, BA-7021), with 225 mL of sterile 0.1% peptone water. Appropriate decimal dilutions of the samples were prepared using the same diluents and plated in duplicate on different

397

Histamine and Histamine-Forming Bacteria

growth media. The growth media were as follows: Arginine decarboxylase agar (ADA) for putrescine producing bacteria; Lysine decarboxylase agar (LDA) for cadaverine producing bacteria and modified Niven’s media for histamine producing bacteria. All agar plates were incubated at 30℃ for 48 h for the mesophilic counts (Niven et al., 1981). A total of 90 isolates from decarboxylase agar plates representing different stages of keropok lekor processing were randomly picked and further streaked on trypticase soy agar (TSA) (Difco) to obtain pure cultures. The presumptive histamine-forming isolates were identified on the basis of morphology, gram stain, endospore stain, catalase and oxidase reaction. Statistical analysis All data collected were analysed by SAS 9.1 statistical package (SAS Institute, Inc. 2002-2003) using one-way analysis of variance (ANOVA). Duncan’s multiple range was used to determine significant differences

among means. All data reported are the means of five replicates. Results TVB and TMA levels in keropok lekor after kneading, boiling and cooling are presented in Figure 1. TVB and TMA levels in keropok lekor after kneading were 7.29 and 3.38 mg/ 100g, respectively. TVB and TMA levels in keropok lekor decreased significantly (p < 0.05) to 4.68 and 1.81 mg/ 100g, respectively after boiling. However, the levels of TMA increased significantly (p < 0.05) the after cooling stage (Figure 1). Putrescine, cadaverine and histamine levels in keropok lekor after kneading, boiling and cooling stage are shown in Figure 2. The levels of putrescine, cadaverine and histamine after kneading were 3.89, 5.05 and 5.92 and after boiling

9 8

Kneading

7

Boiling Cooling

mg/ 100 g

6 5 4 3 2 1 0

TVB

TMA

Fig. 1. Levels of total volatile bases (TVB) and trimethylamine (TMA) in keropok lekor after kneading, boiling and cooling stagea. a Means (SD from five determinations) 9 8

Kneading

Boiling

Cooling

7

ppm

6 5 4 3 2 1 0

Putrescine

Cadaverine

Histamine

Fig. 2. Levels of putrescine, cadaverine and histamine in keropok lekor after kneading, boiling and cooling stagea a Means (SD from five determinations)

m. a. r. nor-khaizura et al.

398

lysine decarboxylase agar and modified Niven’s media were picked randomly at different stages of keropok lekor processing (after kneading, boiling and cooling stage) are presented in Table 1. After kneading stage, isolates isolated were members of family Enterobacteriaceae and genus Staphylococcus spp., Pseudomonas spp. and Micrococcus spp. Enterobacteriaceae and Staphylococcus spp. were identified to have the ability to produce putrescine, cadaverine and histamine. Members of the Pseudomonas genus were found to produce putrescine and cadaverine. Members of the genus Micrococcus spp. were identified to produce histamine. After the boiling stage, only members of the genus Staphylococcus and Micrococcus were isolated. Genus isolated after cooling stage were similar with the genus isolated after kneading and boiling stage except for the absent of Pseudomonas spp.

were 2.94, 4.65 and 5.64 ppm, respectively. After the cooling stage, the levels of putrescine, cadaverine and histamine were 4.72, 5.88 and 6.97 ppm, respectively, which were significantly higher (p < 0.05) than levels after the boiling stage. Putrescine, cadaverine and histamine producers show the counts ranging from 3 to 6 log10 cfu/g. The numbers of microorganisms producing putrescine, cadaverine and histamine in keropok lekor decreased significantly (p < 0.05) after boiling stage (Figure 3). Isolates producing putrescine, cadaverine and histamine decreased significantly (p < 0.05) after kneading and boiling stage from 5.81 to 3.73, 5.59 to 3.57 and 6.80 to 4.26 log10 cfu/g, respectively. After cooling stage isolates producing putrescine (5.05 log10 cfu/g), cadaverine (4.34 log10 cfu/g) and histamine (5.27 log10 cfu/g) were increased significantly (p < 0.05). A total of 90 isolates from arginine decarboxylase agar, 8.00 Kneading

7.00

Boiling

Cooling

Log10 cfu/g

6.00 5.00 4.00 3.00 2.00 1.00 0.00

Putrescine-forming bacteria

Cadaverine-forming bacteria

Histamine-forming bacteria

Fig. 3. Putrescine, cadaverine and histamine-forming bacteria in keropok lekor after kneading, boiling and cooling stagea a Means (SD from five determinations) Table 1. Presumptive identification of isolates from Lysine Decarboxylase Agar (LDA), Arginine Decarboxylase Agar (ADA) and Niven’s Agar plates from keropok lekor at different stages of processing (after kneading, boiling and cooling stage).

Types of Biogenic amines producers

Processing stage Kneading

Boiling

Cooling

Putrescine (ADA)

Enterobacteriaceae Staphylococcus spp. Enterobacteriaceae Staphylococcus spp. Staphylococcus spp. Pseudomonas spp.

Cadaverine (LDA)

Enterobacteriaceae Staphylococcus spp. Enterobacteriaceae Staphylococcus spp. Staphylococcus spp.

Histamine (Niven’s agar)

Enterobacteriaceae Staphylococcus spp. Enterobacteriaceae Staphylococcus spp. Micrococcus spp. Staphylococcus spp. Pseudomonas spp. Micrococcus spp. Micrococcus spp.

Histamine and Histamine-Forming Bacteria

Discussion The changes in the levels of total volatile bases (TVB), trimethylamine (TMA) and biogenic amines producers shared a similar trend at the different stages of keropok lekor processing (after kneading, boiling and cooling), whereby it revealed a significant decrease after boiling and a significant increase after the cooling stage. The TVB and TMA levels were indicated as high after the kneading stage. This high level in TVB was most likely due to a combination of microbiological and autolytic deamination of amino acids. Meanwhile, the TMA level might be generated by a complete reduction of TMAO to TMA by microorganisms (Hansen et al., 1996, Ababouch et al., 1996). This is also in line with the findings of other researchers (Hebard et al., 1982; Fernandez-Salguero and Mackie, 1987; Huss, 1988; Krzymien and Elias, 1990; Koutsoumanis and Nychas, 1999) which had also reported higher levels of TMA due to decomposition of TMAO, as a result of bacterial spoilage and enzymatic activity under favourable temperature and pH conditions. Moreover, higher TMA values might also be associated with the post-harvest handling conditions involving bacterial contamination of fish muscle (Chytiri et al., 2004). A significant reduction in the TVB and TMA levels were observed after the boiling stage. The reduction could be due to the elevated temperature during the boiling process, where the TVB and TMA could leach out into the boiling water. This is in agreement with the findings reported by Kilinc and Cakli (2005), which stated that the TVB and TMA level is reduced by the heat treatment use in the processing. The samples of keropok lekor indicated very low levels of biogenic amines after the kneading stage. The presence of biogenic amines can be attributed to the presence of biogenic microorganisms which produce exogenous decarboxylases (Rawles et al., 1996). Biogenic amines in food have also been related to the low quality of the raw materials, in which a high proliferation of microorganisms occurs (Suzzi and Gardini, 2003). Besides that, other authors such as Maijala et al., 1995a, Eerola et al., 1998a, Komprda et al., (2001) have confirmed the important role played by the microbiological quality of the raw materials, with other variables such as pH, aw, NaCl, etc., which can impose important effects on the production of biogenic amines in fish products. Different genus of bacterial, which are capable of decarboxylating amino acids, have been isolated from fish muscle (Taylor, 1986; Yoshinaga and Frank, (1982); Morii et al., 1988; Okuzumi et al., 1990). These include mesophilic and psychrophilic bacteria; most of them possess more than one decarboxylase enzyme (Taylor and Sumner, 1986). In this study, biogenic amines producers were isolated in high num-

399

bers after the kneading stage. This reflected the quality of fish used, as well as other raw materials and the environment in which the keropok lekor processing was carried out. Members of the Enterobacteriaceae family and the genus of Pseudomonas spp., Staphylococcus spp. and Micrococcus spp. were isolated after the kneading stage. Pseudomonas species are parts of the natural micro-flora of fish and fish products (Hubbs, 1991; Jay, 2000), and are known to be strong producers of biogenic amines (Suzzi and Gardini, 2003). Their decarboxylase activity is well known in fish products (Lehane and Olley, 2000; Jorgensen et al., 2000). Members of the Enterobacteriaceae family are also known to be involved in the production of putrescine, cadaverine and histamine (DurluOzkaya et al., 2001). The sources of Enterobacteriaceae, Staphylococcus spp. and Micrococcus spp. might have come from the raw materials used in the keropok lekor processing, such as minced fish and starch. Ansorena et al. (2002) stated that the microorganisms responsible for the decarboxylation reactions might constitute parts of the natural population of the food. In addition, the contamination due to the handling process at this stage might also be responsible for the occurrence of these microorganisms. It has also been suggested that the hygienic quality of the meat may also enhance biogenic amines levels in sausages (Suzzi and Gardini, 2003). The boiling process did not reduce the levels of biogenic amines significantly even though the number of the biogenic amines producers had been significantly reduced. These results are consistent with those of Lehane and Olley (2000) and Fletcher et al. (1998) who reported that subsequent cooking or processing of a spoiled fish revise the relationship between bacterial numbers and biogenic amines production by reducing or removing the microbial population, without affecting the biogenic amines levels significantly. After the boiling stage, isolates belonging to the Gram positive genus were isolated. According to Liston (1992) and Jay (2000), Gram negative bacteria are usually predominant in food stored at 0-25℃, whereas Gram positive bacteria are predominant in foods stored at elevated temperatures. Staphylococcus spp. and Micrococcus spp were isolated after the boiling stage. Histidine decarboxylase activity was observed in some species belonging to the genus Staphylococcus spp. and Micrococcus spp. (Rodriguez-Jerez et al., 1994b; Martuscelli et al., 2000). The cooling process of keropok lekor, done at the room temperature for 1 to 2 h, was responsible for the increase in the TVB, TMA, biogenic amines level and the number of biogenic amines producers. For this, Andersen (1997) reported that formation of biogenic amines could be induced by short-term temperature abuse. Furthermore, the ability of biogenic amines producers to increase significantly may

m. a. r. nor-khaizura et al.

400

lead to an increase in biogenic amines levels (Rodtong et al., 2005). Biogenic amines producers, isolated after the cooling stage, were those organisms which probably survived the boiling process and might come from a contamination that occurred during the cooling process. Enterobacteriaceae and Staphylococcus spp. are recognized as putrescine, cadaverine and histamine producers, whereas Micrococcus spp. are only known to produce histamine. In addition, some members of the Enterobacteriaceae family possess high decarboxylase activity, particularly in relation to the production of putrescine and cadaverine (Suzzi and Gardini, 2003). They also produce considerable levels of histamine (Halasz et al., 1994). Although these microorganisms are usually present in low amounts in the final product, improper storage of raw materials can lead to their proliferation (Suzzi and Gardini, 2003). Furthermore, it is the enzyme release (and not the microbial cells) which is responsible for the accumulation of biogenic amines and this action can continue in the absence of viable cell (Bover-Cid et al., 2001b). The formation of specific amines in the fish product also depends on a particular microbial flora as well as their counts (Paleologos et al., 2004). The high levels of biogenic amines in food may be correlated to the presence of high counts of spoilage organisms due cross-contamination at various stages of processing (Paleologos et al., 2004). In the processing of keropok lekor (after kneading, boiling and cooling stages), the TVB, TMA and biogenic amine levels in this fish product were found to be below the regulatory permitted levels. The TVB levels during the three stages ranged from 4 to 7 mg/ 100g, which were below the regulatory permitted levels of 30 to 35 mg/ 100g (Sikorski et al., 1989). The TMA levels ranged from 2 to 3 mg/ 100g, which were also below the regulatory permitted levels of 10 to 15 mg/ 100g (Connell, 1995). In addition, biogenic amines levels of keropok lekor were lower than the regulatory permitted levels (50 ppm) (FDA, 1996) with putrescine, cadaverine and histamine levels ranged from 2 to 4, 4 to 6 and 5 to 7 ppm, respectively.

treatment during boiling could also improve the quality of keropok lekor. References Ababouch, L. H., Souibri, L., Rhaliby, K., Ouadhi, O., Battal, M. and Busta, F. F. (1996). Quality changes in sardines (Sardina pilchardus) stored in ice and at ambient temperature. Food Microbiol., 13, 123-132. Andersen, E. M. (1997). Quality assurance on board fishing vessels. In Fish Inspection, Quality Control, and HACCP: A Global Focus, ed. by R. E. Martin, R. L. Collette, J. W. Slavin, J.W., Proceedings of the Conference 19-24 May 1996, Arlington, VA: Technomic. pp. 427-436. Ansorena, D., Montel, M. C., Rokka, M., Talon, R., Eerola, S., Rizzo, A., Raemaekers, M. and Demeyer D. (2002). Analysis of biogenic amines in northern and southern European sausages and role of flora in amine production. Meat Sci., 61, 141-147. Berna Kilinc and Sukran Cakli, (2005). Determination of the shelf life of sardine (Sardina pilchardus) marinades in tomato sauce stored at 4℃. Food Cont., 16, 639-644. Botta, J. R., Lauder, J. T. and Jewer, M. A. (1984a). Effect of methodology on total volatile basic nitrogen (TVB-N) determination as an index of quality of fresh Atlantic cod (Gadus morhua). J. Food Sci., 49, 734-736. Botta, J. R., Lauder, J. T. and Jewer, M. A. (1984b). Effect of methodology on the total volatile basic nitrogen (TVB-N) determination as an index of quality of fresh Atlantic cod (Gadus morhua). J. Food Sci., 49, 734-736. Bover-Cid, S., Izquierdo-Pulido, M. and Vidal-Carou, M. C., (2001b). Effect of the interaction between a low tyramine-producing Lactobacillus and proteolytic staphylococci on biogenic amine production during ripening and storage of dry sausages. Int. J. Food Microbiol., 65, 113- 123. Cheow, C. S. (1998). Effect of protein, salt, sugar and MSG on the microstructural, rheological and physicochemical properties of fish cracker (keropok). PhD Thesis, Universiti Putra Malaysia. Chytiri, S., Chouliara, I., Savvaidis, I. N. and Kontominas, M. G. (2004). Microbiological, chemical and sensory evaluation of iced whole and filleted aquacultured rainbow trout. Food Microbiol.,

Conclusion Boiling process have been determined to be able to reduce TVB, TMA and putrescine, cadaverine and histamineforming bacteria but not for putrescine, cadaverine and histamine content. However, cooling process at room temperature revealed a significant increase for TVB, TMA, putrescine, cadaverine and histamine and their-forming bacteria. Therefore, proper cooling procedure need to be emphasized in order to assure that TVB, TMA and putrescine, cadaverine and histamine-forming bacteria will not rise back after boiling process. A good quality of raw materials and effective heat

21, 157-165. Connell, J. J. (1995). Control of Fish Quality, 4th Edition. pp. 157, 159-160. Furnham, Surrey, UK: Fishing News Books Limited. Conway, E. J. and Byrne, A. (1933). An absorption apparatus for the micro-determination certain volatile substances 1. The microdetermination of ammonia. Biochem. J., 27, 419- 429. Durlu-Ozkaya, F., Ayhan, K., Vural, N. (2001). Biogenic amine produced by Enterobacteriaceae isolated from meat products. Meat Sci., 58, 163-166. Eerola, S., Maijala, R., Roig-Sagués, A. X., Salminen, M. and Hirvi, T.K. (1998a). Biogenic amines in dry sausages as affected

Histamine and Histamine-Forming Bacteria by starter culture and contaminant amine-positive Lactobacillus. J. Food Sci., 61, 1243-1246. FDA 1996. Fish and fisheries products hazards & controls guide: first edition. US Food and Drug Administration, Center for Food Safety and Applied Nutrition, Office of Seafood. Washington D.C.

401 Kyaw, Z. Y., Yu, S. Y., Cheow, C. S. and Dzulkifly, M. H. (1999). Effect of steaming time on linear expension of fish crackers (Keropok). J. Sci. Food Agric., 79, 1340. Lehane, L. and Olley, J., (2000). Histamine fish poisoning revisited. Int. J. Food Microbiol., 58, 1-37.

Fernandez-Salguero, J. and Mackie, I. M., (1987). Comparative

Liston J. (1992). Bacterial spoilage of seafood. In Developments in

rates of spoilage of fillets and whole fish during storage of had-

food science, Vol. 30 quality assurance in the fish industry, ed. by

dock (Melanogammus aeglefinus) and herring (Clupea arengus)

H.H. Huss, M. Jakobsen and J. Liston (ed), Proceedings of an in-

as determined by the formation of non-volatile and volatile

ternational conference. Copenhagen, Denmark: Elsevier Science

amines. Int. J. Food Sci. Technol., 22, 385-390.

Publishing. pp. 93-105.

Fletcher, G. C., Summers, G. and van Veghel, P. W. C. (1998). Lev-

Maijala, R., Eerola, S., Lievonen, S., Hill, P. and Hirvi, T. (1995a).

els of histamine and histamine-producing bacteria in smoked fish

Formation of biogenic amines during ripening of dry sausages

from New Zealand markets. J. Food Prot., 61 (8), 1064-1070.

as affect by starter cultures and thawing time of raw materials. J.

Halasz, A., Barath, A., Simon-Sarkadi, L. and Holzapfel, W. (1994). Biogenic amines and their production by microorganisms in food. Trends Food Sci. Technol., 5, 42-48. Hansen, L. T., Gill, T., Rontved, S. D. and Huss, H. H. (1996). Importance of autolysis and microbiological activity of cold-smoked salmon. Food Res. Int., 29, 181-188. Hebard, C. E., Flick, G. J. and Martin, R. E. (1982). Occurrence and significance of trimetylamine oxide and its derivates in fish and

Food Sci., 69, 1187-1190. Martuscelli, M., Crudele, M.A., Gardini, F. and Suzzi, G. (2000). Biogenic amine formation and oxidation by Staphylococcus xylosus strains from artisanal fermented sausages. Letters Appl. Microbiol., 31, 228-232. Mietz, J. L. and Karmas, E. (1978). Polyamines and histamine content in rockfish, salmon, lobster and shrimp as an indicator of decomposition. J. Assoc. Off. Anal. Chem., 61, 139-145.

shellfish. In Chemistry and biochemistry of marine food products,

Morii, H., Cann, D.C. and Taylor, L.Y. (1988). Histamine formation

ed. by R. E. Martin, G. P. Flick and D. R., Ward. Westport, CT:

by luminous bacteria in mackerel stored at low temperatures. Nip.

AVI. pp. 149-304. Hubbs, J. (1991). Fish: microbiological spoilage and safety. Food Sci. Technol. Today, 5, 166-173.

Sui. Gak., 54, 299-305. Ng C. S. and Low L. K. (1992). Determination of trimetylamine oxide (TMAO-N), trimethylamine (TMA-N), total volatile basic

Huss, H. H. (1988). Fresh fish-quality and quality changes FAO

nitrogen (TVB-N) by conway’s microdiffusion method. In Labo-

fisheries series No. 29. Rome: FAO Danish International Devel-

ratory Manual on Analytical Methods and Procedures for Fish

opment Agency.

and Fish Products (2nd ed.) ed. by M. Katsutoshi and S. J. Low,

Hwang, D. F., Chang, S. H., Shiau, C. Y. and Chai, T. (1997). High performance liquid chromatographic determination of biogenic amines in fish implicated in food poisoning. J. Chromatogr. B, 693, 23-30. Jay, J. M., (2000). Modern Food Microbiology 6th ed. Gaithersburg, Maryland: Aspen Publishers, Inc. Jorgensen, L. V., Dalgaard, P., Huss, H. H., (2000). Multiple compound quality index for cold-smoked salmon (Salmon salar) developed by multivariate regression of biogenic amines and pH. J. Agric. Food Chem., 48, 2448-2453.

Marine Fisheries Research Department Southeast Asian Fisheries Development Center Singapore. pp. B 3.1- B 3.7. Niven, C. F., Jeffrey, M. B. and Corlett, D. A. (1981). Differential plating medium for quantitative detection of histamine-producing bacteria. Appl. Env. Microbiol., 41, 321-322. Okozumi, M., Fukumoto, I. and Fujii, T. (1990). Changes in bacterial flora and polyamine contents during storage of horse mackerel meat. Nip. Sui. Gak., 56, 1307-1312. Paleologos, E. K., Savvaidis I. N. and Kontominas M. G. (2004). Biogenic amines formation and its relation to microbiological and

Komprda, T., Neznalova, J., Standara, S. and Bover-Cid, S. (2001).

sensory attributes in ice-stored whole, gutted and filleted Medi-

Effect of starter culture and storage temperature on the content

terranean Sea bass (Dicentrarchus labrax). Food Microbiol., 21,

of biogenic amines in dry fermented sausages poliean. Meat Sci.,

549-557.

59, 267-276. Koutsoumanis, K. and Nychas, G. J. E. (1999). Chemical and sen-

Rawles, D. D., Flick, G. J. and Martin, R. E. (1996). Biogenic amines in fish and shellfish. Adv. Food Nutr. Res., 39, 329-364.

sory changes associated with microbial flora of Mediterranean

Riebroy, S., Benjakul, S., Visessanguan, W., Kijrongrojana, K. and

bogue (Boops boops) stored aerobically at 0, 3, 7, and 10℃.

Tanaka, M. (2004). Some characteristic of commercial Som-fug

Appl. Env. Microbiol., 65, 698-706.

produced in Thailand. Food Chem., 88, 527-535.

Krzymien, M. E. and Elias, L. (1990). Feasibility study on the de-

Rodriguez-Jerez, J. J., Mora-Ventura, M. T., Lopez-Sabater, E. I.

termination of fish freshness by trimethylamine head space analy-

and Hernandez-Herrero, M. M. (1994b). Histidine, lysine and

sis. J. Food Sci., 55, 1228-1231.

ornithine decarboxylase bacteria in salted semi-preserved ancho-

m. a. r. nor-khaizura et al.

402 vies. J. Food Prot., 57, 784-787. Rodtong, S., Nawong, S. and Yongsawatdigul, J. (2005). Histamine accumulation and histamine-forming bacteria in Indian anchovy (Stolephorus indicus). Food Microbiol., 22, 475-782. SAS Institute Inc. (2002-2003). SAS User’s Guide: Statistics. SAS Institute Inc. Siaw, C. L., Yu, S. Y. and Chen, S. S. (1979). Studies on Malaysia fish cracker effect of sago, tapioca and wheat flour on acceptability, In Proceedings of Second Symposium of the Federation of Asian and Oceanian Biochemists. Kuala Lumpur. pp. 128-136. Siaw, C. L., Idrus, A. Z. and Yu, S. Y. (1985). Intermediate technology for fish cracker (‘keropok’) production. J. Food Technol., 20, 17-21. Sidaway, E. P. and Balasingam, M. (1971). Keropok in fish processing industry in West Malaysia, MARDI, Serdang, Selangor, Report no. 42. Sikorski, Z. E., Kolakowska, A. and Burt, J. R. (1989). Post harvest biochemical and microbial changes. Seafood: resources, nutritional composition and preservation. Boca Raton, Florida: CRC Press Inc.

Suzzi, G. and Gardini, F. (2003). Biogenic amines in dry fermented sausage: a review. Int. J. Food Microbiol., 88, 41-54. Taylor, S.L. (1986). Histamine food poisoning: toxicology and clinical aspects. Crit. Rev. Toxicol., 17, 91-128. Taylor, S. L. and Sumner, S. S. (1986). Determination of histamine, putrescine, and cadaverine. In Seafood Quality Determination, ed. by D. E. Kramer and J. Liston, Amsterdam: Elsevier. pp. 235-245. Villareal, B. P. and Pozo, R. (1990). Chemical composition and ice spoilage of Albacore (Thunnus alalunga). J. Food Sci., 55(3), 678-682. Yoshinaga, D. H. and Frank, H. A., (1982). Histamine-producing bacteria in decomposing skipjack tuna (Katsuwonus pelamis). Appl. Env. Microbiol., 44, 447-452. Yu, S.Y., Mitchell, J.R. and Abdullah, A. (1981). Production and acceptability testing of fish crackers prepared by extrusion method. J. Food Technol., 16, 57-58. Yu, S.Y. (1992). Oreochromis mossambicus in fish crackers (keropok). ASEA- Food J., 7 (1).