Biogenic Amine Survey and Organoleptic Changes in Fresh, Stored, and Temperature-Abused Blue®Sh (Pomatomus Saltatrix)

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Journal of Food Protection, Vol. 62, No. 9, 1999, Pages 1033±1037 Copyright ᮊ, International Association of Milk, Food and Environmental Sanitarians

Biogenic Amine Survey and Organoleptic Changes in Fresh, Stored, and Temperature-Abused Blue®sh (Pomatomus saltatrix)

TODD M. GINGERICH,* TATIANA LORCA, GEORGE J. FLICK, MERLE D. PIERSON, AND HAROLD M. MCNAIR

Department of Food Science and Technology, Virginia Tech, Blacksburg, Virginia 24061, USA

MS 98-237: Received 4 September 1998/Accepted 3 January 1999

ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/62/9/1033/2007656/0362-028x-62_9_1033.pdf by guest on 28 September 2021

Changes in histamine, putrescine, and cadaverine concentrations in blue®sh ®lets (Pomatomus saltatrix) stored at 5, 10, and 15ЊC were determined using high-performance liquid chromatography. An organoleptic assessment was conducted simultaneously with the biogenic amine analyses. The histamine levels found in fresh blue®sh obtained from wholesale seafood distributors ranged between Ͻ1 ppm and 99 with an average of 39 ppm. Putrescine and cadaverine were not found in fresh blue®sh. Fish ®llets stored at each of the three temperatures developed histamine. The greatest accumulation of histamine was observed in ®sh stored at 15ЊC, which developed histamine levels as high as 2,200 ppm. Putrescine levels increased at each temperature during storage. Cadaverine was present only in uninoculated blue®sh stored at 15ЊC. Histamine achieved higher levels in blue®sh pieces inoculated with Morganella morganii, which demonstrates that blue®sh support bacterial histamine formation. Histamine levels at each temperature exceeded the 50-ppm advisory level established by the Food and Drug Administration before 100% sensory rejection. Standard plate counts increased during storage of ®sh at all temperatures, but the correlation between histamine levels and standard plate count was not signi®cant.

The ingestion of relatively large amounts of histamine, histamine, only M. morganii, K. pneumoniae, and H. alvei sometimes present in decomposed ®sh of certain species, is have been isolated from ®sh causing scombroid poisoning thought to cause an illness known as histamine poisoning (16). or scombroid poisoning (12). Histamine poisoning in ®sh In addition to histamine levels in ®sh, concentrations is often referred to as scombroid poisoning because spoiled of other biogenic amines may be of importance in scom- ®sh of the families Scombroidae and Scomberesocidae, broid poisoning. The biogenic amines putrescine and ca- such as tuna and mackerel, are often implicated in hista- daverine are thought to play a synergistic role with histamine poisoning outbreaks. There have, however, been out- mine in the occurrence of scombroid poisoning. It is pos- breaks associated with other nonscombroid species such as sible that this potentiation of histamine stems from the in- mahi mahi, blue®sh, and sail®sh (10, 15). hibition of the histamine detoxi®cation processes in the Histamine belongs to a group of chemical compounds body by cadaverine and putrescine (15). known as biogenic amines. Biogenic amines are generally This work was conducted to observe levels of hista- formed by decarboxylation of free amino acids in tissue or mine, putrescine, and cadaverine in stored blue®sh (Po- by amination and transamination of aldehydes and ketones matomus saltatrix) using a high-performance liquid chro- (13). The major source of biogenic amines in ®sh is the matography (HPLC) method. Because of the high histidine decarboxylation of amino acids by certain decarboxylase level present in blue®sh tissue, there is a possibility of his- enzymes. These enzymes, either native in the raw material tamine development in the species, and in fact several out- or produced in the ®sh by bacteria, are speci®c for the for- breaks of histamine poisoning have resulted from ingestion mation of each individual biogenic amine (5). Most re- of blue®sh (17). A known histamine-forming bacteria spe- searchers agree that the majority of biogenic amines present cies, M. morganii, was inoculated onto a portion of the in ®sh are a result of exogenous decomposition of amino stored blue®sh pieces in order to observe the bacteria's pro- acids by bacteria possessing decarboxylase enzymes (18). duction of histamine. Sensory data were accumulated, Most of the bacteria that produce histamine in ®sh and along with the chemical analysis, to study the risk of con- ®sh products belong to the family Enterobacteriaceae (7). sumer acceptance of blue®sh containing high levels of his- Bacterial species known to possess the ability to convert tamine. histidine to histamine include Enterobacter aerogenes, E. cloacae, Hafnia alvei, Klebsiella pneumoniae, Morganella MATERIALS AND METHODS morganii, Proteus vulgaris, and Vibrio alginolyticus (7). Storage of ®sh. Fresh blue®sh (P. saltatrix) was obtained Despite the ability of many species of bacteria to produce from wholesale markets in Hampton, Va. After purchase, the ®sh was transported on ice to the Food Science and Technology De- * Author for correspondence. Present address: 8404 Angler's Pointe Drive, partment at Virginia Polytechnic Institute and State University in Temple Terrace, FL 33637, USA. Tel: 813-899-0523; Blacksburg, Va. Upon arrival in Blacksburg, the whole blue®sh E-mail: [email protected]. were ®lleted and cut into 100 samples approximately 50 g in 1034 GINGERICH ET AL. J. Food Prot., Vol. 62, No. 9 weight. The samples were placed in sterile Whirl-Pak bags prior Experimental design and statistical analysis. Four samples to storage. The bags were placed on trays and incubated at 5ЊC, of fresh ®sh were subjected to biogenic amine analysis and stan- 10ЊC, and 15ЊC for up to 7 days or until 100% sensory rejection. dard plate counts before each storage study began. The biogenic amine analysis, standard plate counts, and sensory analysis were Inoculation procedure. The M. morganii organisms used in conducted daily on one sample each of both the inoculated and this study were ATCC 25830, batch 95±02SV obtained from the the control samples at each of the three storage temperatures. This American Type Culture Collection, Rockville, Md. One milliliter resulted in a maximum of six samples tested per day, one sample of the M. morganii stock culture was placed in 9 ml trypticase from each treatment, each of which was discarded after analysis. soy broth (TSB; Difco Laboratories, Detroit, Mich.) and incubated Samples from each treatment were tested daily up to either the for 24 h at 37ЊC. After incubation, 1 ml of the 24-h culture was day of 100% sensory rejection or the seventh day of storage, inoculated into a second TSB tube and incubated for 4 h at 37ЊC. whichever came ®rst. After the day when 100% sensory rejection A 4-h incubation selected after growth curve measurements con- occurred, no more samples from that treatment were tested. The ®rmed that the inoculum was in the log phase of growth. The HPLC biogenic amine analysis was conducted twice for each of

growth curve for M. morganii was derived from hourly absor- the extracted samples, resulting in a maximum of 12 injections Downloaded from http://meridian.allenpress.com/jfp/article-pdf/62/9/1033/2007656/0362-028x-62_9_1033.pdf by guest on 28 September 2021 bance readings (660 nm) of culture tube (TSB incubated at 37ЊC) per day. The entire experiment was replicated three times. turbidity and simultaneous plating (trypticase soy agar, TSA; Dif- All statistical tests were performed using the SAS statistical co) of the incubating culture. A 0.1-ml aliquot of the 4-h M. mor- program (SAS Institute Inc., SAS Campus Drive, Cary, N.C.). ganii culture (106 CFU/ml) was dispensed onto the surface of half Logistic regression was performed on the sensory data. A split- (50) of the ®sh samples using a sterile pipette. After inoculation, plot design with mixed models was used to analyze the biogenic both the inoculated samples and uninoculated control samples amine levels. A correlation analysis was conducted on histamine were stored at the previously described conditions. levels and standard plate counts.

Sensory analysis. Sensory analysis was conducted for each RESULTS AND DISCUSSION temperature during the storage periods for 7 days or until spoilage was detected by 100% of the panelists. The sensory panel con- Biogenic amine formation. The histamine levels sisted of at least 12 volunteers experienced in seafood products. found in fresh blue®sh obtained from wholesale seafood The panelists were presented with a fresh reference during each distributors ranged between Ͻ1 ppm and 99 ppm with an day of analysis and were asked to make an acceptance decision average of 39 ppm. Some of the ®sh obtained from the based on the appearance and smell of each sample. The fresh distributors exceeded the Food and Drug Administration references consisted of seven samples of thawed blue®sh muscle (FDA) established 50-ppm guidance level (1). The high lev- tissue. The references, which were obtained from the same lot as els of variability between ®sh samples can be attributed to the test sample, were kept frozen until needed for sensory anal- many factors including a range of storage temperatures, dif- ysis. A new reference sample was thawed on each day of the 7 ferent harvest times, harvest methods, and differences in days of analysis and discarded after that sensory session. microbial ¯ora present on the ®sh. Chemical analysis. Biogenic amine analysis for histamine, Histamine was found in the uninoculated blue®sh sam- cadaverine, and putrescine was conducted using the following ex- ples stored at 5ЊC and 10ЊC (Table 1). The histamine con- traction and HPLC procedure. Fish pieces (50 g) to be analyzed centrations of those samples were quite variable and did were homogenized using a Waring blender. A 10-g portion of the not appreciably increase over time. Histamine levels in the homogenate was extracted three times with 20 ml of 5% wt/vol uninoculated ®sh stored at 5ЊC ranged between 18 and 100 trichloroacetic acid (Fisher Scienti®c, Fair Lawn, N.J.). After cen- ppm and between 12 and 52 ppm in the uninoculated ®sh trifugation (6,000 ϫ g, 10ЊC) for 10 min, the extracts were com- stored at 10ЊC. Some of this variability may be attributed bined and ®ltered through glass wool. The sample pH was ad- to histamine formation prior to sample collection. Hista- justed to 8.9 using 0.1 M borate buffer (Fisher). The sample was mine levels were found to increase in the uninoculated sam- then derivatized with 4.0 mM ¯uorescamine (Sigma Chemical ples stored at 15ЊC, reaching 938 ppm in the samples stored Co., St. Louis, Mo.) in acetonitrile and agitated for 30 s. for 3 days (Table 1). This concentration of histamine sug- The derivatized sample was analyzed with a Perkin-Elmer series 410 LC pump equipped with a Phenomenex IB-Sil 100 ϫ gests the presence of histamine-forming bacteria. 4.6-mm 5.0-␮m (C18) reverse-phase (RP)-HPLC column fol- The ®sh samples inoculated with M. morganii and lowed by detection with a Hitachi model F100 ¯uorescence spec- stored at 5ЊC had histamine concentrations ranging from 16 trophotometer. Five microliters of the derivatized extract was in- to 116 ppm, but no de®nite increase over time was ob- jected at a ¯ow rate of 1.5 ml/min using a gradient consisting of served (Table 2). Histamine levels did increase in inoculat- 0.02 M phosphate buffer, pH 7.2/acetonitrile; 80/20 for 2 min to ed samples at both 10ЊC and 15ЊC accumulating 338 and 50/50 in 5 min (mobile phase chemicals obtained from Fisher). 2,200 ppm, respectively (Table 2). These data are in agree- The derivative of each sample was analyzed twice. For the ¯uo- ment with previous studies concluding that most of the bac- rescence detection, an excitation wavelength of 390 nm and an teria responsible for high levels of histamine in ®sh are emission wavelength of 475 nm was used. mesophilic bacteria belonging to the Enterobacteriaceae Standard plate counts. Standard plate counts were con- (7). Optimum temperature for histamine production in skip- Њ ducted daily on samples prior to biogenic amine analysis. A 9- jack tuna was found to be 37.8 C (8). cm2 area of each sample was swabbed with a sterile calcium al- Fresh blue®sh did not contain detectable levels of pu- ginate-tipped swab. The swab tip was broken off into a 9-ml trescine or cadaverine. Putrescine formation did occur dur- 0.01% peptone blank and then serially diluted. The dilutions were ing storage at all temperatures, and each increasing incre- plated onto TSA and incubated for 48 h at 37ЊC. ment of temperature showed a signi®cant rise in putrescine J. Food Prot., Vol. 62, No. 9 BIOGENIC AMINES IN BLUEFISH 1035

TABLE 1. Sensorial acceptance and histamine, putrescine, and cadaverine levels during storage of uninoculated blue®sh (n ϭ 3) Time Standard (days) Temperature plate count % acceptance Histaminea Putrescinea Cadaverinea

0 Ð 1.5E6 Ϯ 8.6E5 Ð 39 Ϯ 29 NDb ND 1 5 4.1E4 Ϯ 2.1E4 74 Ϯ 1 58 Ϯ 28 ND ND 1 10 5.4E4 Ϯ 9.2E4 62 Ϯ 6 52 Ϯ 33 ND ND 1 15 2.8E6 Ϯ 2.6E6 44 Ϯ 14 35 Ϯ 26 ND ND 2 5 2.0E4 Ϯ 5.8E2 96 Ϯ 4 50 Ϯ 43 ND ND 2 10 5.4E5 Ϯ 6.1E5 47 Ϯ 13 41 Ϯ 7 ND ND 2 15 7.3E6 Ϯ 5.1E6 12 Ϯ 12 55 Ϯ 39 51 Ϯ 39 ND 3 5 1.8E4 Ϯ 6.1E3 79 Ϯ 9 45 Ϯ 63 ND ND 3 10 1.1E8 Ϯ 1.7E8 18 Ϯ 3 44 Ϯ 21 34 Ϯ 40 ND

3 15 4.2E7 Ϯ 2.1E7 0 938 Ϯ 200 96 Ϯ 58 50 Ϯ 62 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/62/9/1033/2007656/0362-028x-62_9_1033.pdf by guest on 28 September 2021 4 5 5.3E4 Ϯ 4.9E4 77 Ϯ 9 42 Ϯ 43 9 Ϯ 8 ND 4 10 2.6E7 Ϯ 1.4E7 5 Ϯ 3 12 Ϯ 14 104 Ϯ 85 ND 5 5 1.3E9 Ϯ 1.8E9 57 Ϯ 23 100 Ϯ 11 8 Ϯ 11 ND 5 10 4.2E7 Ϯ 3.7E7 0 33 Ϯ 37 99 Ϯ 107 ND 6 5 4.7E7 Ϯ 6.6E7 37 Ϯ 12 18 Ϯ 10 14 Ϯ 12 ND 7 5 8.0E9 Ϯ 1.4E10 25 Ϯ 0 25 Ϯ 44 30 Ϯ 8 ND a Measured in ppm. b ND, not detected (limit of detection ϭ 1 ppm). production (P Ͻ 0.0001). Putrescine levels of 30 ppm or samples that were inoculated with M. morganii (P Ͻ greater were found at all storage temperatures. Overall, pu- 0.0001). This would be expected from histidine-decarbox- trescine levels increased with time, reaching a maximum ylase enzymes produced by the bacteria. M. morganii is level of 150 ppm in M. morganii-inoculated samples stored well documented as a histamine-producing organism and at 10ЊC (Table 2). Cadaverine, however, was found only in has been isolated from ®sh responsible for scombrotoxic uninoculated ®sh stored at 15ЊC, in which 50 ppm was incidences (2, 11). Greater differences in histamine for- present on the third day of storage (Table 1). In past re- mation between inoculated and uninoculated blue®sh were search, positive correlation was found between expert sen- observed in ®sh stored at higher temperatures (P Ͻ sory decisions for accept/reject quality and levels of pu- 0.0001). This indicates that histamine-decarboxylase en- trescine and cadaverine in the product (14). zyme activity, enzyme production, or both were greater at Bacteriological effects. Overall, there was a signi®- the higher temperatures. cantly greater production of histamine in those blue®sh Putrescine production was greater in those samples in-

TABLE 2. Sensorial acceptance and histamine, putrescine, and cadaverine levels during storage of Morganella morganii-inoculated blue®sh (n ϭ 3) Time Standard (days) Temperature plate count % acceptance Histaminea Putrescinea Cadaverinea

0 Ð 1.5E6 Ϯ 8.5E5 Ð 39 Ϯ 29 NDb ND 1 5 3.5E4 Ϯ 3.8E4 77 Ϯ 5 102 Ϯ 10 ND ND 1 10 1.9E5 Ϯ 5.8E4 52 Ϯ 34 43 Ϯ 17 ND ND 1 15 7.4E6 Ϯ 1.2E7 26 Ϯ 32 286 Ϯ 261 10 Ϯ 7 ND 2 5 1.2E6 Ϯ 3.8E4 95 Ϯ 7 69 Ϯ 74 ND ND 2 10 7.6E5 Ϯ 9.3E5 37 Ϯ 33 54 Ϯ 13 ND ND 2 15 1.6E8 Ϯ 2.0E8 0 2154 Ϯ 10 64 Ϯ 10 ND 3 5 1.9E4 Ϯ 1.3E4 79 Ϯ 20 69 Ϯ 43 9 Ϯ 12 ND 3 10 2.0E7 Ϯ 1.3E7 24 Ϯ 5 31 Ϯ 12 35 Ϯ 20 ND 3c 15 5.0E6 Ϯ 0 0 2200 Ϯ 0 97 Ϯ 0 ND 4 5 3.6E5 Ϯ 2.3E5 57 Ϯ 12 47 Ϯ 57 83 Ϯ 72 ND 4 10 2.0E7 Ϯ 9.8E6 3 Ϯ 3 338 Ϯ 13 150 Ϯ 4 ND 5 5 6.5E8 Ϯ 9.2E8 52 Ϯ 12 116 Ϯ 0 8 Ϯ 11 ND 6 5 2.6E8 Ϯ 4.5E8 19 Ϯ 9 80 Ϯ 36 13 Ϯ 12 ND 7 5 1.3E9 Ϯ 1.4E10 19 Ϯ 6 16 Ϯ 15 77 Ϯ 8 ND a Measured in ppm. b ND, not detected (limit of detection ϭ 1 ppm). c n ϭ 1. 1036 GINGERICH ET AL. J. Food Prot., Vol. 62, No. 9 oculated with M. morganii than the control samples (P Ͻ oculated blue®sh stored at 15ЊC (Table 2). Histamine levels 0.025). This suggests that M. morganii contains the en- on storage days 2 and 3 exceeded 2,000 ppm, compared to zymes necessary for production of putrescine. The presence levels Ͻ1,000 ppm in the uninoculated samples. However, of cadaverine in the control samples stored at 15ЊC and not these levels occurred when there was 0% acceptance. In- in the inoculated samples stored at 15ЊC could be the result oculated blue®sh stored for 1 day at 15ЊC (Table 2) con- of competitive inhibition of cadaverine-producing organ- tained histamine levels above 300 ppm, still a possible ill- isms by M. morganella. ness hazard, but the percent acceptance was below 30%. In The standard plate counts follow a general increasing inoculated blue®sh stored at 10ЊC (Table 2), histamine lev- trend in all of the storage temperatures. The highest counts els only exceeded 100 ppm after being judged unacceptable were found in the samples stored for 7 days at 5ЊC (Tables by 90% of the panelists. Histamine levels in uninoculated 1 and 2). Counts of 8.0E9 CFU/cm2 and 1.3E9 CFU/cm2 ®sh stored at 10ЊC (Table 1) never exceeded 100 ppm. were found in the uninoculated and inoculated samples, re- Histamine levels at 5ЊC were variable but failed to

spectively. A correlation analysis was conducted on hista- reach the levels observed in spoiled ®sh at the 15ЊC storage Downloaded from http://meridian.allenpress.com/jfp/article-pdf/62/9/1033/2007656/0362-028x-62_9_1033.pdf by guest on 28 September 2021 mine levels and standard plate counts. There was no sig- conditions (Tables 1 and 2). Levels of histamine were often ni®cant correlation found between the change in histamine above the 50-ppm advisory level established by the FDA concentrations and the change in total plate count at each (1), and in some cases above 100 ppm in both the inocu- temperature (P Ͻ 0.64 at 5ЊC, P Ͻ 0.90 at 10ЊC, and P Ͻ lated and uninoculated blue®sh. 0.24 at 15ЊC). This indicates that either histamine-forming Putrescine and cadaverine are thought to augment bacteria made up only a small part of the ¯ora or that en- scombrotoxic incidences by interfering with histamine me- zyme production or activity was affected by temperature. tabolism in the human intestine (9). A study on cadaverine and putrescine potentiation of histamine poisoning in guin- Sensory analysis. The sensory analysis was conducted ea pigs concluded that cadaverine levels similar to those simultaneously with biogenic amine analysis to determine found in scombrotoxic ®sh potentiated lethal effects of his- whether a population may be at risk for accepting blue®sh tamine (4). In the same study, putrescine levels commonly with high histamine levels. As expected, the percentage of found in spoiled ®sh were not found to potentiate histamine sensory volunteers accepting the ®sh decreased with each poisoning of the guinea pigs. If this is the case, it is im- successive day of storage. Overall, the inoculated blue®sh portant to understand levels of other biogenic amines, be- had lower percentages of acceptance values (P Ͻ 0.0001). sides histamine, that occur in ®sh. This study concluded It is dif®cult to ascertain if this decrease in acceptance was that putrescine formation up to 150 ppm was possible in the result of higher levels of histamine present in the in- blue®sh, and that cadaverine levels of 50 ppm were possible oculated ®sh or if it was the result of other decomposition in cases of severe decomposition. products. In past studies, histamine alone has not been In this study, histamine was found in all blue®sh, in- found as an acceptable indicator of ®sh spoilage. Foods cluding the fresh ®sh. This shows that this particular ®sh containing unusually high levels of histamine may not ap- species is at risk for development of histamine. The study pear outwardly spoiled (17). Frank et al. (7) reported that concluded that although putrescine was not present in fresh skipjack tuna judged decomposed by sensory analysis fre- samples, it could be formed during storage temperatures as quently had histamine levels of less than 50 ppm. Increased low as 5ЊC. Cadaverine formation was only evident at the microbial loads may have caused increases in volatile highest storage temperature of 15ЊC. This research shows amines that have been widely used as freshness indicators that blue®sh may contain the biogenic amines histamine, in some species of marine ®sh and result in strong odors putrescine, and cadaverine. during ®sh decomposition (6). Acceptance levels were higher in those ®sh stored at lower temperatures (Tables 1 ACKNOWLEDGMENTS and 2), and the values for percent acceptance were signif- icantly different between each storage temperature (P Ͻ This research was sponsored by NOAA of®ce of Sea Grant, U.S. Department of Commerce under federal grant no. NA90AA-D-SGO45 to 0.0001). the Virginia Graduate Marine Science Consortium, and the Virginia Sea Consumer risk. Bartholomew et al. (3) reviewed 250 Grant College Program. This work was issued in furtherance of Cooper- ative Extension work, Virginia Polytechnic Institute and State University, cases of scombroid poisoning in Great Britain from 1976 Virginia State University, and the U.S. Department of Agriculture coop- to 1986 and observed that the presence of greater than 20 erating: C. Clark Jones, Director, Virginia Cooperative extension, Virginia mg/100 g (200 ppm) in ®sh is a good indication of its Tech, Blacksburg, Va.; Lorenza W. Lyons, Administrator, 1890 Extension potential to cause scombrotoxic ®sh poisoning. The FDA Program, Virginia State University, Petersburg, Va. states that most illness-causing ®sh have contained hista- REFERENCES mine concentrations above 20 mg/100 g (200 ppm), often above 50 mg/100 g (500 ppm), but they set a guidance level 1. Anonymous. 1996. 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