Histamine and Histamine-Forming Bacteria in Keropok Lekor (Malaysian Fish Sausage) During Processing

Food Sci. Technol. Res., 15 (4), 395–402, 2009

Histamine and Histamine-Forming Bacteria in Keropok lekor (Malaysian Fish Sausage) during Processing

1* 2 3 4 Mahmud Ab Rashid nor-khaizura , Hassan zaiton , Bakar jamiLah , Rahmat Ali Gulam ruSuL and 3 Mohammad Rashedi iSmaiL-FitrY

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 3 Department of Food Technology, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 Serdang, Selangor, 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 been used; these include total volatile bases (TVB), trimeth- Keropok lekor is a popular and highly relished fish prod- ylamine (TMA) and biogenic amines (Botta et al., 1984a, uct in Malaysia. Keropok lekor normally prepared with a 1984b; Hebard et al., 1982; Mietz and Karmas, 1978). TVB mixture of fish to starch at 1:1 ratio, added with salt, sugar and TMA are widely used to determine fish product qual- and monosodium glutamate (msg). The processing of kero- ity. Analysis for TVB involves the estimation of all volatile pok lekor involves mainly five stages comprises of mincing amines produce during spoilage. Meanwhile, TMA are re- the fish meat, mixing the minced fish with other ingredients, sulted from the reduction of trimethylamine-oxide (TMAO) kneading the dough, boiling and cooling before it is pack- by bacterial activity and intrinsic enzymes. It is often used as aged. At present, most of manufacturers producing keropok an index of freshness of fish and fish products (Hush 1988; lekor carry out the processing manually with little mecha- Villareal and Pozo, 1990). The levels of TVB and TMA that nization. This product can be easily found in night market, have been considered as the upper limit in fishery products hawkers stall and also most of the school canteen. Keropok are 30 – 35 mg/ 100 g (Hush, 1988; Sikorski et al., 1989; lekor are served as appetizer or snack with local special chilli Connell, 1995) and 10 – 15 mg/ 100 g (Sikorski et al., 1989; sauce. Connell, 1995). While, biogenic amines especially histamine, In fish products, a number of spoilage indicators have putrescine and cadaverine, have been suggested as indicators of spoilage for some foods, such as fresh fish, meat and veg- *To whom correspondence should be addressed. etables (Riebroy et al., 2004). The importance of estimating E-mail: [email protected] the concentration of biogenic amines in fish and fish products 396 m. a. r. nor-khaizura et al. is related to their impact on human health and food quality. micro-burette unit, until the green color turns pink. Blank To the present, information on chemical quality of kero- test was carried out using 1 mL of 4% TCA instead of sample pok lekor is very limited. Most studies carried out previously solution (Conway and Byrne, 1933). on keropok lekor were focus on the physical characteristics Trimetylamine (TMA) Sealing agent was applied to of the final product (Siaw et al., 1985; Kyaw et al., 1999; Conway’s unit. 1 mL of inner ring solution was pipette into Cheow, 1998; Yu, 1992), and on the processing and formula- inner ring. Then, 1 mL of sample solution was pipette into tion of keropok lekor (Sidaway and Balasingam, 1971; Siaw outer ring. 1 mL of neutralized 10% formaldehyde (R&M et al., 1979; Yu et al., 1981). The objective of the study was Chemicals) was pipette into the outer ring and the outer ring to determine levels of total volatile bases (TVB), trimeth- solutions were gently mixed. The Conway’s unit with cover ylamine (TMA), putrescine, cadaverine and histamine and was slanted and 1 mL of saturated K2CO3 solution (Ajax their forming bacteria at different stages of keropok lekor Chemicals) was pipette into the outer ring. The Conway’s processing (kneading, boiling and cooling stage). unit was immediately closed and tightened with clip. The outer ring solution was mixed gently and allowed to stand for Materials and Methods 60 min at 37℃ in an incubator. The inner ring solution was Sample collection Five hundred grams samples were titrated against 0.02N Hydrochloric acid (Fisher Scientific) collected at different processing stages for 5 replications. The using a micro-burette unit, until the green color turned pink. processing stages are after kneading the dough, after boil- Blank test was carried out using 1 mL of 4% TCA instead ing and after cooling stage. The kneading process was done sample solution (Conway and Byrne, 1933). manually at ambient temperature. Furthermore, the boiling Biogenic amines analysis The samples were ground process was carried out in the boiler at 100℃ for 10 min and in a Waring blender for 3 min. 5 g sample was transferred cooling process was done at room temperature, where boiled to a 50 mL centrifuge tube and homogenized with 20 mL of keropok lekor was arranged on the stainless steel table and 6% trichloroacetic acid (TCA) for 3 min. The homogenate allowed to cool for about 1 to 2 h. Samples were obtained was centrifuged at 8000 × g, for 10 min at 4℃ and filtered using sterile utensils and were placed into sterile plastic through Whatman No. 2 filter paper. The filtrate was placed bags, which were properly labelled and dated. Samples were in a volumetric flask and made up to 50 mL. Samples of brought to the laboratory in a pre-chilled container with standard biogenic amine solutions and 2 mL aliquots of the crushed ice (4 ± 1℃) and analysed within 24 h. sample extracts were derivatized with benzoyl chloride ac- Determination of Total Volatile Bases (TVB) and Trimeth- cording to the previously described method (Hwang et al., ylamine (TMA) Total volatile bases (TVB) and trimethyl- 1997). The benzoyl derivatives were dissolved in 1 mL of amine (TMA) were determined using Conway’s Microdiffu- methanol and 20 μl aliquots were used for high-performance sion Method (Ng and Low, 1992). liquid chromatography (HPLC) injection. Sample preparation Two grams of sample were Amines were determined by using HPLC (Shimadzu, Ja- weighed on aluminium foil and transferred into a mortar pan, consisting of a Model LC-6A pump, Model SPD-6A UV and grinded. 8mL of 4% Trichloroacetic acid (TCA) (Fisher detector set at 254 nm, a Model C-R6A chromatopac integra- Chemicals) was added and grinded. The mixture was allowed tor). A LiChrosopher 100RP – 18 reverse phase column (5 to stand for 30 min at ambient temperature and grinded oc- μm, 125 × 4 mm I.D., E.Merck) was used for the separation. casionally. The mixture was than centrifuged (Kubota, 2100) The gradient elution program was set at 0.8 mL/min, start- at 3000 rpm for 10 min. The filtrate was kept at -20℃ in a ed with a methanol-water mixture (50:50, v/v) for 0.5 min. freezer before proceeding to the next step. The program proceeded linearly to methanol-water (85:15, Total Volatile Bases (TVB) Sealing agent was applied v/v), with a flow rate of 0.8 mL/min over 6.5 min. This was to Conway’s unit. 1 mL of inner ring solution (Appendix C) followed by the same composition and flow rate for 5 min, was pipette into inner ring. Then, 1 mL of sample solution then a decreased over 2 min to methanol-water (50:50, v/v) was pipette into outer ring. The Conway’s unit with cover at 0.8 mL/min. was slanted and 1 mL of saturated Potassium carbonate so- Isolation of histamine- forming bacteria Twenty lution (K2CO3) (Ajax Chemicals) was pipette into the outer five grams of keropok lekor at each processing stages was ring. The Conway’s unit was immediately closed and tight- aseptically transferred to a sterile stomacher bag and pum- ened with clip. The outer ring solution was mixed gently and melled for 1 min in a stomacher (Seaward Stomacher 400, allowed to stand for 60 min at 37℃ in an incubator (Binder, BA-7021), with 225 mL of sterile 0.1% peptone water. Ap- BD 53). After incubation, the inner ring solution was titrated propriate decimal dilutions of the samples were prepared against 0.02N Hydrochloric acid (Fisher Scientific) using a using the same diluents and plated in duplicate on different Histamine and Histamine-Forming Bacteria 397 growth media. The growth media were as follows: Arginine among means. All data reported are the means of five repli- decarboxylase agar (ADA) for putrescine producing bacteria; cates. Lysine decarboxylase agar (LDA) for cadaverine producing bacteria and modified Niven’s media for histamine produc- Results ing bacteria. All agar plates were incubated at 30℃ for 48 h TVB and TMA levels in keropok lekor after kneading, for the mesophilic counts (Niven et al., 1981). A total of 90 boiling and cooling are presented in Figure 1. TVB and TMA isolates from decarboxylase agar plates representing differ- levels in keropok lekor after kneading were 7.29 and 3.38 ent stages of keropok lekor processing were randomly picked mg/ 100g, respectively. TVB and TMA levels in keropok and further streaked on trypticase soy agar (TSA) (Difco) lekor decreased significantly (p < 0.05) to 4.68 and 1.81 mg/ to obtain pure cultures. The presumptive histamine-forming 100g, respectively after boiling. However, the levels of TMA isolates were identified on the basis of morphology, gram increased significantly (p < 0.05) the after cooling stage (Fig- stain, endospore stain, catalase and oxidase reaction. ure 1). Statistical analysis All data collected were analysed by Putrescine, cadaverine and histamine levels in keropok SAS 9.1 statistical package (SAS Institute, Inc. 2002-2003) lekor after kneading, boiling and cooling stage are shown in using one-way analysis of variance (ANOVA). Duncan’s Figure 2. The levels of putrescine, cadaverine and histamine multiple range was used to determine significant differences after kneading were 3.89, 5.05 and 5.92 and after boiling

8 Kneading Boiling 7 Cooling 6 5 00 g 4 mg / 1 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)

8 Kneading Boiling Cooling

ppm 4

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) 398 m. a. r. nor-khaizura et al. were 2.94, 4.65 and 5.64 ppm, respectively. After the cool- lysine decarboxylase agar and modified Niven’s media were ing stage, the levels of putrescine, cadaverine and histamine picked randomly at different stages of keropok lekor process- were 4.72, 5.88 and 6.97 ppm, respectively, which were sig- ing (after kneading, boiling and cooling stage) are presented nificantly higher (p < 0.05) than levels after the boiling stage. in Table 1. After kneading stage, isolates isolated were mem- Putrescine, cadaverine and histamine producers show bers of family Enterobacteriaceae and genus Staphylococcus the counts ranging from 3 to 6 log10 cfu/g. The numbers of spp., Pseudomonas spp. and Micrococcus spp. Enterobac- microorganisms producing putrescine, cadaverine and his- teriaceae and Staphylococcus spp. were identified to have tamine in keropok lekor decreased significantly (p < 0.05) the ability to produce putrescine, cadaverine and histamine. after boiling stage (Figure 3). Isolates producing putrescine, Members of the Pseudomonas genus were found to produce cadaverine and histamine decreased significantly (p < 0.05) putrescine and cadaverine. Members of the genus Micro- after kneading and boiling stage from 5.81 to 3.73, 5.59 to coccus spp. were identified to produce histamine. After the

3.57 and 6.80 to 4.26 log10 cfu/g, respectively. After cooling boiling stage, only members of the genus Staphylococcus stage isolates producing putrescine (5.05 log10 cfu/g), cadav- and Micrococcus were isolated. Genus isolated after cooling erine (4.34 log10 cfu/g) and histamine (5.27 log10 cfu/g) were stage were similar with the genus isolated after kneading and increased significantly (p < 0.05). boiling stage except for the absent of Pseudomonas spp. A total of 90 isolates from arginine decarboxylase agar,

8.00

7.00 Kneading Boiling Cooling

6.00

5.00

cfu/g 4.00 10

Log 3.00

2.00

1.00

0.00 Putrescine-forming Cadaverine-forming Histamine-forming bacteria bacteria 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 De- carboxylase Agar (ADA) and Niven’s Agar plates from keropok lekor at different stages of processing (after kneading, boiling and cooling stage).

Types of Processing stage Biogenic amines producers Kneading Boiling Cooling Putrescine Enterobacteriaceae Staphylococcus spp. Enterobacteriaceae (ADA) Staphylococcus spp. Staphylococcus spp. Pseudomonas spp. Cadaverine Enterobacteriaceae Staphylococcus spp. Enterobacteriaceae (LDA) Staphylococcus spp. Staphylococcus spp. Histamine Enterobacteriaceae Staphylococcus spp. Enterobacteriaceae (Niven’s agar) Staphylococcus spp. Micrococcus spp. Staphylococcus spp. Pseudomonas spp. Micrococcus spp. Micrococcus spp. Histamine and Histamine-Forming Bacteria 399

Discussion bers after the kneading stage. This reflected the quality of The changes in the levels of total volatile bases (TVB), fish used, as well as other raw materials and the environment trimethylamine (TMA) and biogenic amines producers in which the keropok lekor processing was carried out. Mem- shared a similar trend at the different stages of keropok lekor bers of the Enterobacteriaceae family and the genus of Pseu- processing (after kneading, boiling and cooling), whereby it domonas spp., Staphylococcus spp. and Micrococcus spp. revealed a significant decrease after boiling and a significant were isolated after the kneading stage. Pseudomonas species increase after the cooling stage. are parts of the natural micro-flora of fish and fish products The TVB and TMA levels were indicated as high after (Hubbs, 1991; Jay, 2000), and are known to be strong pro- the kneading stage. This high level in TVB was most likely ducers of biogenic amines (Suzzi and Gardini, 2003). Their due to a combination of microbiological and autolytic de- decarboxylase activity is well known in fish products (Lehane amination of amino acids. Meanwhile, the TMA level might and Olley, 2000; Jorgensen et al., 2000). Members of the En- be generated by a complete reduction of TMAO to TMA terobacteriaceae family are also known to be involved in the by microorganisms (Hansen et al., 1996, Ababouch et al., production of putrescine, cadaverine and histamine (Durlu- 1996). This is also in line with the findings of other research- Ozkaya et al., 2001). The sources of Enterobacteriaceae, ers (Hebard et al., 1982; Fernandez-Salguero and Mackie, Staphylococcus spp. and Micrococcus spp. might have come 1987; Huss, 1988; Krzymien and Elias, 1990; Koutsoumanis from the raw materials used in the keropok lekor processing, and Nychas, 1999) which had also reported higher levels of such as minced fish and starch. Ansorena et al. (2002) stated TMA due to decomposition of TMAO, as a result of bacterial that the microorganisms responsible for the decarboxylation spoilage and enzymatic activity under favourable tempera- reactions might constitute parts of the natural population of ture and pH conditions. Moreover, higher TMA values might the food. In addition, the contamination due to the handling also be associated with the post-harvest handling conditions process at this stage might also be responsible for the occur- involving bacterial contamination of fish muscle (Chytiri et rence of these microorganisms. It has also been suggested al., 2004). that the hygienic quality of the meat may also enhance bio- A significant reduction in the TVB and TMA levels were genic amines levels in sausages (Suzzi and Gardini, 2003). observed after the boiling stage. The reduction could be due The boiling process did not reduce the levels of biogenic to the elevated temperature during the boiling process, where amines significantly even though the number of the biogenic the TVB and TMA could leach out into the boiling water. amines producers had been significantly reduced. These re- This is in agreement with the findings reported by Kilinc and sults are consistent with those of Lehane and Olley (2000) Cakli (2005), which stated that the TVB and TMA level is and Fletcher et al. (1998) who reported that subsequent reduced by the heat treatment use in the processing. cooking or processing of a spoiled fish revise the relationship The samples of keropok lekor indicated very low levels between bacterial numbers and biogenic amines production of biogenic amines after the kneading stage. The presence of by reducing or removing the microbial population, without biogenic amines can be attributed to the presence of biogenic affecting the biogenic amines levels significantly. After the microorganisms which produce exogenous decarboxylases boiling stage, isolates belonging to the Gram positive genus (Rawles et al., 1996). Biogenic amines in food have also were isolated. According to Liston (1992) and Jay (2000), been related to the low quality of the raw materials, in which Gram negative bacteria are usually predominant in food a high proliferation of microorganisms occurs (Suzzi and stored at 0-25℃, whereas Gram positive bacteria are pre- Gardini, 2003). Besides that, other authors such as Maijala et dominant in foods stored at elevated temperatures. Staphy- al., 1995a, Eerola et al., 1998a, Komprda et al., (2001) have lococcus spp. and Micrococcus spp were isolated after the confirmed the important role played by the microbiological boiling stage. Histidine decarboxylase activity was observed quality of the raw materials, with other variables such as pH, in some species belonging to the genus Staphylococcus aw, NaCl, etc., which can impose important effects on the spp. and Micrococcus spp. (Rodriguez-Jerez et al., 1994b; production of biogenic amines in fish products. Martuscelli et al., 2000). Different genus of bacterial, which are capable of decar- The cooling process of keropok lekor, done at the room boxylating amino acids, have been isolated from fish muscle temperature for 1 to 2 h, was responsible for the increase in (Taylor, 1986; Yoshinaga and Frank, (1982); Morii et al., the TVB, TMA, biogenic amines level and the number of 1988; Okuzumi et al., 1990). These include mesophilic and biogenic amines producers. For this, Andersen (1997) re- psychrophilic bacteria; most of them possess more than one ported that formation of biogenic amines could be induced decarboxylase enzyme (Taylor and Sumner, 1986). In this by short-term temperature abuse. Furthermore, the ability study, biogenic amines producers were isolated in high num- of biogenic amines producers to increase significantly may 400 m. a. r. nor-khaizura et al. lead to an increase in biogenic amines levels (Rodtong et al., treatment during boiling could also improve the quality of 2005). Biogenic amines producers, isolated after the cooling keropok lekor. stage, were those organisms which probably survived the boiling process and might come from a contamination that References occurred during the cooling process. Enterobacteriaceae and Ababouch, L. H., Souibri, L., Rhaliby, K., Ouadhi, O., Battal, M. Staphylococcus spp. are recognized as putrescine, cadaverine and Busta, F. F. (1996). Quality changes in sardines (Sardina pil- and histamine producers, whereas Micrococcus spp. are only chardus) stored in ice and at ambient temperature. Food Micro- known to produce histamine. In addition, some members biol., 13, 123-132. of the Enterobacteriaceae family possess high decarbox- Andersen, E. M. (1997). Quality assurance on board fishing ves- ylase activity, particularly in relation to the production of sels. In Fish Inspection, Quality Control, and HACCP: A Global putrescine and cadaverine (Suzzi and Gardini, 2003). They Focus, ed. by R. E. Martin, R. L. Collette, J. W. Slavin, J.W., also produce considerable levels of histamine (Halasz et al., Proceedings of the Conference 19-24 May 1996, Arlington, VA: 1994). Although these microorganisms are usually present Technomic. pp. 427-436. in low amounts in the final product, improper storage of raw Ansorena, D., Montel, M. C., Rokka, M., Talon, R., Eerola, S., materials can lead to their proliferation (Suzzi and Gardini, Rizzo, A., Raemaekers, M. and Demeyer D. (2002). Analysis of 2003). Furthermore, it is the enzyme release (and not the biogenic amines in northern and southern European sausages and microbial cells) which is responsible for the accumulation of role of flora in amine production.Meat Sci., 61, 141-147. biogenic amines and this action can continue in the absence Berna Kilinc and Sukran Cakli, (2005). Determination of the shelf of viable cell (Bover-Cid et al., 2001b). The formation of life of sardine (Sardina pilchardus) marinades in tomato sauce specific amines in the fish product also depends on a particu- stored at 4℃. Food Cont., 16, 639-644. lar microbial flora as well as their counts (Paleologos et al., Botta, J. R., Lauder, J. T. and Jewer, M. A. (1984a). Effect of meth- 2004). The high levels of biogenic amines in food may be odology on total volatile basic nitrogen (TVB-N) determination correlated to the presence of high counts of spoilage organ- as an index of quality of fresh Atlantic cod (Gadus morhua). J. isms due cross-contamination at various stages of processing Food Sci., 49, 734-736. (Paleologos et al., 2004). Botta, J. R., Lauder, J. T. and Jewer, M. A. (1984b). Effect of meth- In the processing of keropok lekor (after kneading, boil- odology on the total volatile basic nitrogen (TVB-N) determina- ing and cooling stages), the TVB, TMA and biogenic amine tion as an index of quality of fresh Atlantic cod (Gadus morhua). J. levels in this fish product were found to be below the regula- Food Sci., 49, 734-736. tory permitted levels. The TVB levels during the three stages Bover-Cid, S., Izquierdo-Pulido, M. and Vidal-Carou, M. C., ranged from 4 to 7 mg/ 100g, which were below the regula- (2001b). Effect of the interaction between a low tyramine-pro- tory permitted levels of 30 to 35 mg/ 100g (Sikorski et al., ducing Lactobacillus and proteolytic staphylococci on biogenic 1989). The TMA levels ranged from 2 to 3 mg/ 100g, which amine production during ripening and storage of dry sausages. were also below the regulatory permitted levels of 10 to 15 Int. J. Food Microbiol., 65, 113- 123. mg/ 100g (Connell, 1995). In addition, biogenic amines lev- Cheow, C. S. (1998). Effect of protein, salt, sugar and MSG on the els of keropok lekor were lower than the regulatory permitted microstructural, rheological and physicochemical properties of levels (50 ppm) (FDA, 1996) with putrescine, cadaverine and fish cracker (keropok). PhD Thesis, Universiti Putra Malaysia. histamine levels ranged from 2 to 4, 4 to 6 and 5 to 7 ppm, Chytiri, S., Chouliara, I., Savvaidis, I. N. and Kontominas, M. G. respectively. (2004). Microbiological, chemical and sensory evaluation of iced whole and filleted aquacultured rainbow trout. Food Microbiol., Conclusion 21, 157-165. Boiling process have been determined to be able to re- Connell, J. J. (1995). Control of Fish Quality, 4th Edition. pp. 157, duce TVB, TMA and putrescine, cadaverine and histamine- 159-160. Furnham, Surrey, UK: Fishing News Books Limited. forming bacteria but not for putrescine, cadaverine and hista- Conway, E. J. and Byrne, A. (1933). An absorption apparatus for mine content. However, cooling process at room temperature the micro-determination certain volatile substances 1. The micro- revealed a significant increase for TVB, TMA, putrescine, determination of ammonia. Biochem. J., 27, 419- 429. cadaverine and histamine and their-forming bacteria. There- Durlu-Ozkaya, F., Ayhan, K., Vural, N. (2001). Biogenic amine pro- fore, proper cooling procedure need to be emphasized in or- duced by Enterobacteriaceae isolated from meat products. Meat der to assure that TVB, TMA and putrescine, cadaverine and Sci., 58, 163-166. histamine-forming bacteria will not rise back after boiling Eerola, S., Maijala, R., Roig-Sagués, A. X., Salminen, M. and process. A good quality of raw materials and effective heat Hirvi, T.K. (1998a). Biogenic amines in dry sausages as affected Histamine and Histamine-Forming Bacteria 401

by starter culture and contaminant amine-positive Lactobacillus. J. Kyaw, Z. Y., Yu, S. Y., Cheow, C. S. and Dzulkifly, M. H. (1999). Food Sci., 61, 1243-1246. Effect of steaming time on linear expension of fish crackers (Ker- FDA 1996. Fish and fisheries products hazards & controls guide: opok). J. Sci. Food Agric., 79, 1340. first edition. US Food and Drug Administration, Center for Food Lehane, L. and Olley, J., (2000). Histamine fish poisoning revisited. Safety and Applied Nutrition, Office of Seafood. Washington D.C. 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). Food Sci., 69, 1187-1190. Biogenic amines and their production by microorganisms in food. Martuscelli, M., Crudele, M.A., Gardini, F. and Suzzi, G. (2000). Trends Food Sci. Technol., 5, 42-48. Biogenic amine formation and oxidation by Staphylococcus Hansen, L. T., Gill, T., Rontved, S. D. and Huss, H. H. (1996). Im- xylosus strains from artisanal fermented sausages. Letters Appl. portance of autolysis and microbiological activity of cold-smoked Microbiol., 31, 228-232. salmon. Food Res. Int., 29, 181-188. Mietz, J. L. and Karmas, E. (1978). Polyamines and histamine Hebard, C. E., Flick, G. J. and Martin, R. E. (1982). Occurrence and content in rockfish, salmon, lobster and shrimp as an indicator of significance of trimetylamine oxide and its derivates in fish and 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. Sui. Gak., 54, 299-305. Hubbs, J. (1991). Fish: microbiological spoilage and safety. Food Ng C. S. and Low L. K. (1992). Determination of trimetylamine Sci. Technol. Today, 5, 166-173. 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 Marine Fisheries Research Department Southeast Asian Fisheries performance liquid chromatographic determination of biogenic Development Center Singapore. pp. B 3.1- B 3.7. amines in fish implicated in food poisoning. J. Chromatogr. B, Niven, C. F., Jeffrey, M. B. and Corlett, D. A. (1981). Differential 693, 23-30. plating medium for quantitative detection of histamine-producing Jay, J. M., (2000). Modern Food Microbiology 6th ed. Gaithersburg, bacteria. Appl. Env. Microbiol., 41, 321-322. Maryland: Aspen Publishers, Inc. Okozumi, M., Fukumoto, I. and Fujii, T. (1990). Changes in bacte- Jorgensen, L. V., Dalgaard, P., Huss, H. H., (2000). Multiple com- rial flora and polyamine contents during storage of horse mack- pound quality index for cold-smoked salmon (Salmon salar) de- erel meat. Nip. Sui. Gak., 56, 1307-1312. veloped by multivariate regression of biogenic amines and pH. J. Paleologos, E. K., Savvaidis I. N. and Kontominas M. G. (2004). Agric. Food Chem., 48, 2448-2453. 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. Rawles, D. D., Flick, G. J. and Martin, R. E. (1996). Biogenic Koutsoumanis, K. and Nychas, G. J. E. (1999). Chemical and sen- 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- 402 m. a. r. nor-khaizura et al.

vies. J. Food Prot., 57, 784-787. Suzzi, G. and Gardini, F. (2003). Biogenic amines in dry fermented Rodtong, S., Nawong, S. and Yongsawatdigul, J. (2005). Histamine sausage: a review. Int. J. Food Microbiol., 88, 41-54. accumulation and histamine-forming bacteria in Indian anchovy Taylor, S.L. (1986). Histamine food poisoning: toxicology and (Stolephorus indicus). Food Microbiol., 22, 475-782. clinical aspects. Crit. Rev. Toxicol., 17, 91-128. SAS Institute Inc. (2002-2003). SAS User’s Guide: Statistics. SAS Taylor, S. L. and Sumner, S. S. (1986). Determination of histamine, Institute Inc. putrescine, and cadaverine. In Seafood Quality Determination, Siaw, C. L., Yu, S. Y. and Chen, S. S. (1979). Studies on Malaysia ed. by D. E. Kramer and J. Liston, Amsterdam: Elsevier. pp. fish cracker effect of sago, tapioca and wheat flour on acceptabil- 235-245. ity, In Proceedings of Second Symposium of the Federation of Villareal, B. P. and Pozo, R. (1990). Chemical composition and ice Asian and Oceanian Biochemists. Kuala Lumpur. pp. 128-136. spoilage of Albacore (Thunnus alalunga). J. Food Sci., 55(3), Siaw, C. L., Idrus, A. Z. and Yu, S. Y. (1985). Intermediate technol- 678-682. ogy for fish cracker (‘keropok’) production. J. Food Technol., 20, Yoshinaga, D. H. and Frank, H. A., (1982). Histamine-producing 17-21. bacteria in decomposing skipjack tuna (Katsuwonus pelamis). Sidaway, E. P. and Balasingam, M. (1971). Keropok in fish process- Appl. Env. Microbiol., 44, 447-452. ing industry in West Malaysia, MARDI, Serdang, Selangor, Re- Yu, S.Y., Mitchell, J.R. and Abdullah, A. (1981). Production and ac- port no. 42. ceptability testing of fish crackers prepared by extrusion method. Sikorski, Z. E., Kolakowska, A. and Burt, J. R. (1989). Post harvest J. Food Technol., 16, 57-58. biochemical and microbial changes. Seafood: resources, nutri- Yu, S.Y. (1992). Oreochromis mossambicus in fish crackers (kero- tional composition and preservation. Boca Raton, Florida: CRC pok). ASEA- Food J., 7 (1). Press Inc.