Histamine Formation and Honeycombing

During Decomposition of Skipjack Tuna,

Katsuwonus pelamis, at Elevated Temperatures

HILMER A. FRANK, DERRICK H. YOSHINAGA, and WAI-KIT NIP

Introduction Tomiyasu and Zenitani, 1957; Kimata, tine quality control procedure by most
1961; Arnold and Brown, 1978). of the tuna canning industry (Lieber and
Most fish decompose rapidly unless Fresh tuna and other scombroid fIsh Taylor, 1978).
some method of preservation is institut- are essentially devoid of histamine Many other indices have been em-
ed soon after they are caught. One ma- (Geiger et aI., 1944; Geiger, 1948; Har- ployed to measure spoilage in fIsh (Tomi-
jor cause of decomposition is the varied dy and Smith, 1976; Fernandez-Salguero yasu and Zenitani, 1957; Lassen, 1965;
reservoir of spoilage bacteria contained and Mackie, 1979) but they contain sub- Martin et aI., 1978), including sensory
by the fIsh and present in the environ- stantial amounts of free histidine, ex- assessments (Shewan et aI., 1953; Burt
ment. An extensive literature is availa- ceeding 1 g per 100 g of skipjack tuna et aI., 1975), the formation of com-
ble on the distribution and classifIcation tissue (Lukton and Olcott, 1958). It is pounds such as volatile acids (Hillig,
of the spoilage organisms as well as the generally agreed that the histamine 1954, 1956a), trimethylamine (Farber
natural microflora of many kinds of ma- found in scombroid fIsh is formed by and Lerke, 1961; Martin et aI., 1978),
rine fIsh (Griffiths, 1937; Tomiyasu and bacteria that can decarboxylate histidine hypoxanthine (Burt, 1977: Martin et al..
Zenitani, 1957; Shewan, 1961, 1962; (Shifrine et aI., 1959; Kimata, 1961: 1978), volatile reducing substances (Far-
Shewan and Hobbs, 1967; Shewan, Ferencik, 1970; Edmunds and Eitenmil- ber and Lerke, 1961) and ethanol (Lerke
1977). Considerable interest has been ler, 1975; Taylor et aI., 1977; Arnold and Huck, 1977) and high bacterial
directed toward the decomposition of and Brown, 1978; Omura et aI., 1978; counts (Tomiyasu and Zenitani, 1957:
scombroid fIsh (family Scombridae), Taylor et aI., 1979). A variety of such Farber and Lerke. 1961: Lerke et al..
particularly in mackerel, sardines, and bacteria, particularly Enterobacteri- 1965; Martin et al.. 1978). For a number
several types of tuna where spoilage is aceae, recovered from spoiled scom- of years the tuna canning industry also
associated with high levels of histamine broid fish are considered to be responsi- has used honeycomb formation, a con-
in the fIsh (Williams, 1954; Hillig, 1956a; ble for their decomposition and the ele- dition caused by the breakdown of con-
vated histamine observed (Geiger, 1955; nective tissue (Hillig.1956b; Otsu, 1957:
Mossel, 1968; Lerke et aI., 1978; Arnold Lassen, 1965; Tanikawa, 1971; Finch
and Brown, 1978). and Courtney, 1976), as an index of
Because histamine is heat stable, decomposition.
some workers have suggested that the The present investigation concerns
ABSTRACT-Decomposition was studied histamine content would be suitable as a the relationship between histamine for-
in skipjack tuna, Katsuwonus pelamis, caught quantitative index of prior microbial mation and decomposition in skipjack
in Hawaiian waters. Fresh skipjack tuna tis-
sue was practically devoid of histamine spoilage in canned tuna (Geiger, 1944; tuna, Katsuwonus pelamis, and is part of
(about 0.1 mgllOO g tuna), but this com- Williams, 1954; Ferencik et aI., 1961; a broader study of spoilage in tuna caught
pound formed readily when whole .fish were Ienistea, 1973). At present, histamine near the Hawaiian Islands. This study
incubated at moderate and elevated temper- evaluation is used voluntarily as a rou- shows that the optimum temperature for
atures. Histamine formation was optimum at
]7.SOC (1000F) and was dependent upon
histamine formation in skipjack tuna is
microbial activity. Honeycombing, a condi- 37.8°C (lOOOF), and that the optimum
tion characterized by the destruction of con- for honeycombing is 32.2°C (90°F).
nective tissue, was evaluated in incubated Moreover, histamine formation is de-
skipjack tuna and had an optimum tempera- The authors are with the Department of Food pendent upon microbial activity. but
ture of ]2.:?C (90° Fj. Honeycomb forma- Science and Human Nutrition, University of
tion occurred in the presence of antibiotics honeycombing can occur in the pres-
Hawaii. Honolulu, HI 96822. This article is
that inhibited microbial activity and hista- Journal Series No. 2568 of the Hawaii Institute ence of antibiotics that are inhibitory to
mine formation. of Tropical Agriculture and Human Resources. microbial growth.

October 1981, 4](10) 9

 Materials and Methods tion of honeycombing throughout the Table 1.-Scale lor quantitative evaluation 01 honeycomb-
ing in skipjack tuna.
fish (Table 1). Honeycombing ratings Score 1 Description
Fish represent mean evaluation scores taken a No honeycombing in any part of fish
Skipjack tuna. each weighing about from duplicate experiments for each set 1 Very slight honeycombing in belly, dorsal line or
blood meat but not in loins
1.8-2.3 kg (4-5 pounds), were caught in of conditions tested. Honeycombing is 2 Slight honeycombing in belly, dorsal line, blood
nearby ocean waters (mean tempera- seen mainly as pitted sponge-like depos- meat and in parts of anterior loins
3 Moderate honeycombing in belly, entire dorsal
ture about 75°F or 24°C). delivered live its between loins and often as indenta- line, blood meat and some loin sections
to the ational Marine Fisheries Service tions of the loin surfaces. In cases of 4 Moderate-to-extensive honeycombing in belly,
entire dorsal iine and. blood meat, and moderate
research facility at Kewalo Basin on advanced honeycombing. the connec- honeycombing in all loins
5 Extensive honeycombing in all parts of fish, in-
Oahu, Hawaii. and held for about 12-IR tive tissue appears vacuolated. and trans- cluding the loins. Connective tissue has a sponge-
hours in storage tanks fed by recirculat- verse sections of the loin resemble a like appearance

ing fresh seawater. The Ilsh were re- vacant honeycomb (Hillig. 1956b; Otsu, 'Intermediate scores (e.g., 0.5, 1.5, etc.) can be assigned
where appropriate.
moved from the tanks, allowed to expire J957).
by being kept for 5-10 minutes in ice-
chilled seawater, and transported in
crushed ice to the Department of Food
Science and Human Nutrition at the
University of Hawaii for use in experi-
ments. Normally about 1 hour elapsed
between expiration of the fish and the
initiation of laboratory incubations.
These precautions prevented any unde-
sired postmortem spoilage changes dur-
ing handling before incubation.
Incubation
The fish were placed in separate poly-
ethylene bags containing 4- 5 I of 1l1-
tered fresh seawater and held for the
desired time in a temperature-controlled
water bath.
Precooking
Following incubation, the tuna were
eviscerated and decapitated, and each
side was cut into sections (Fig. I). The
number of sections obtained depended
upon size; fish weighing 1.8-2.3 kg (4-5
pounds) yielded 5 sections. and smaller
fish could be divided into 3-4 sections.
The sectioned fish were given a low-
pressure steam precook of 15 minutes at
I04.4°C (220°F) in a home-style pres-
sure cooker. In commercial processing,
the purpose of precooking is to coagu-
late the flesh protein to aid removal of
the skin and bones during cleaning and
to facilitate cutting the loins into pieces
suitable for canning (Lassen. J 965; Ba-
con. 1971; Finch and Courtney, 1976).
Honeycombing
LEFT SIDE RIGHT SIDE
A~ter precooking, the tuna were
cooled thoroughly, and honeycomb for-
mation was evaluated by two experi-
enced individuals using a Ilve-point Figure 1. - Numbering scheme for identi-
scale based on the degree and distribu- lication of lish sections.

10 Marine Fisheries Review

Histamine Content of Tuna chloride (A. H. Robbins. Richmond. Table 2. - Histamine content of fresh skipjack tuna.

Va.). Fish were incubated for 24 hours at Histamine Img/100 g tunal

Precooked fish sections were cleaned, and fish section number'
comminuted twice in a household meat 35°C (95°F), a temperature that is in- Trial no. 1 2 3 4 5
grinder and analyzed for histamine as termediate between the optima for his- 1 0.06 0.07 0.06 0.08 0.09
described by Staruszkiewicz et al. (1977) tamine formation and honeycombing in 2 0.12 0.11 009 0.12 0.06
3 0.11 010 010 0.10 0.07
and in AOAC (1975) (Sections 18.060- skipjack tuna. 4 0.14 017 008 0.09 0.13

18.062). Ten g of each section were Preliminary experiments revealed 5 0.23 0.17 0.19 011 0.09

extracted with methanol, passed through that slight histamine formation occurred Average 0.13 0.12 0.10 0.10 0.09

in areas of the fish that had not been 'From Figure 1

an anion exchange resin to remove in-
terfering compounds, derivatized with reached by antibiotics, especially in sec-
0- phthalaldehyde, and the histamine
tion 1. To facilitate penetration of the
measured fluorometrically. The hista- antibiotics to all tuna tissue, the gills and
mine content reported for each section viscera were removed and the fish sev-
of fish represents the mean value of ered between sections 2 and 3. Each Table 3.-Histamine content of skipjack tuna incubated
eight estimations taken from duplicate piece was put in a separate polyethylene 24 hours at various temperatures.

determinations by two technicians for bag containing seawater plus antibiotics Histamine (mg/100 g lunal
Temp. and fish section number'
both sides of the section. and placed in the water bath. After in-
°C OF 2 3 4 5
Because histamine levels were not cubation for 24 hours at 35°C (95°F),
156 60 0.21 018 0.17 018 0.15
uniform for all sections of the same fish analyses were conducted for histamine, 21.1 70 2.80 1.05 0.96 0.99 0.84
honeycombing, and the presence of mi- 239 75 74.5 650 325 2.46 4.95
(see Tables 3, 4), it was difficult some- 26.7 80 102 6.99 159 4.51 290
times to compare tuna that had been croorganisms. 29.4 85 114 72.5 ,
56.0 52.2 ,
71.5
32.2 90 248 41.3 45.2
given different treatments. However, this 350 95 369 241 84.4 591 596
Results 37.8 100 643 540 472 479 534
problem was overcome by considering 40.6 105 354 236
3
185 255
each fish as a single system whose his- Histamine Formation 43.3110 1.47'
48.9 120 0.62'
tamine load could be expressed by its From Figure 1
composite histamine content. Compos- Fresh skipjack tuna contained essen- 1

'Very small fish; only 3 sections.

ite histamine concentrations (mg/100 g tially no free histamine; in most cases 3Small fish; 4 sections.
'Sectioning was not possible because the fish disinte-
tuna) reported for some fish (see Tables only about 0.1 mg/lOO g was present in grated during incubation. Histamine estimations were
4,7) are calculated as Ithe total amount any fish section (Table 2). made from composites of each side of the fish.

(mg) of histamine present in all fish Table 3 shows the effect of incubation
sections/total weight (g) of all fish sec- temperature on histamine formation in
tions I x 100. skipjack tuna. Very little histamine had
formed in 24 hours at 2J.1 °C (70°F)
Microbiological Examination and below, but at 23.9°C (75°F) a small
Microbial counts were made with tis- amount of histamine was present usually had histamine levels that were
sue taken from tuna section 2. Samples throughout most of the fish, with a sub- nearly as high as in section 1.
were diluted with sterile 0.1 percent stantial level (74.5 mg/100 g) in the Table 4 shows the rates of histamine
peptone (BBL) and inoculated on trypti- anteriormost section 1. The optimum formation during incubation at the op-
case soy agar (BBL); colonies were temperature for histamine production timum temperature, 37.8°C (lOOoF). A
counted after incubation for 2-3 days at was 37.8°C (lOOoF) where levels of 472 lag period of 6-12 hours elapsed before
37°C (98.6°F). Gram stains of tuna tis- to 643 mg/100 g were found in all sec- significant histamine production was
sue and seawater incubation liquid also tions. At higher temperatures, hista- detected in section 1; at 18 hours con-
were examined microscopically for the mine formation decreased, and at siderable histamine was found in most
presence of microorganisms. 43.3°C (llOOF) and above the tuna tis- sections, with greater concentrations
sue underwent extensive deterioration, occurring in the anterior part of the fish.
Antibiotics but very little histamine was present. After 24 hours the histamine level was
The inhibitory effect of antibiotics on A characteristic pattern of histamine very high throughout the fish, ranging
histamine formation and honeycombing distribution was observed in this study. from 261 to 481 mg/lOO g in each sec-
was studied by incubating tuna in sea- The earliest indication of histamine oc- tion. Assessment of histamine forma-
water containing 160 units per ml of curred in fish section 1, and the hista- tion from composite histamine values
Penicillin G (Calbiochem ' , Los Angeles) mine level remained highest in that sec- given in the righthand column of Table 4
and 0.1 mg per ml Tetracycline hydro- tion throughout incubation. The other also shows an initial 12- hour lag and the
fish sections had less histamine, arranged changing production rate that followed.
in a gradually decreasing gradient to- Therefore, composite histamine values
ward the posterior end of the fish. The will be used below to express histamine
'Mention of trade names or commercial firms
does not imply endorsement by the National belly flaps (not included in Tables 2 and formation in terms of the entire fIsh (see
Marine Fisheries Service, NOAA. 3) were exceptions to this gradient and Table 7).

October 1981, 43(10) 11

 Table 4.-Histamine formation in skipjack tuna incubated at 37.8°C (100°F). Table 5. - Honeycomb formation in skipjack tuna incu-
bated 24 hours at various temperatures.
Histamine Img/1 00 9 tuna)
Composite
and fish section number' 2 Honey- Honey-
Time histamine Temperature Temperature
(h) combing combing
2 3 (hours) 4 5 (mg/100 9 tuna) DC OF score! 0c OF score'
o 0.13 0.12 0.10 0.10 0.09 0.11
156 60 o 35.0 95 30-40
6 047 0.43 0.51 0.52 0.55 0.50
21.1 70 05 37.8 100 30
12 421 6.13 3.69 3.91 6.72 15.1
18 213 49.5 21.1 20.7 31.7 67.3
239
267
75
80
05
2.0
40.6
43.3
105
110
1.5,
24 481 367 424 261 289 343
29.4 85 15-20 489 120
'From Figure 1. 322 90 40
, Sum of histamine in all sections Img)
Composite histamine = x 100. 'See Table 1
Total weight of fish sections (g) 'Fish disintegrated; honeycomb evaluation impossible.

Samples of loin tissue taken from tuna duced by about one-half (to 75.6 mg/ Table 6. - Honeycomb formation in skipjack tuna incubated
at 32.2°C (90 0 )F.
incubated IS and 24 hours (Table 4) had 100 g) but honeycombing was unaffect-
Time Honey- Time Honey-
total microbial counts of 2.5X 10; and ed (score = 3.5). However. when uptake in combing in combing
2.SX 10;/g. respectively. Cultures isolat- of the antibiotics was improved by cut- hours score' hours score'
ed from tuna incubated for 24 hours ting the flsh between sections 2 and 3. o 0 22.5 4.0-4.5
7.5 1.0-1.5 30 45-5.0
were mainly gram-negative. facultatively histamine production was essentially in- 15 15-2.0 37.5 5.0
anaerobic rods (Yoshinaga. 1979) and signiflcant (1.62 mg/IOO g). Honey- 'See Table 1
will be the subject of another manu- combing. on the other hand, was fairly
script. extensive (score = 3.5-4.0) after 24
hours and apparently not inhibited by
Honeycombing
the antibiotics.
Table 5 shows the effect of tempera- Microbial counts from the loin tissue Table 7.-Effect of antibiotics on honeycombing and his-
ture on honeycombing in skipjack tuna. and microscopic examination of the sea- tamine formation in skipjack tuna incubated 24 hours at
35°C (95° Fl.
Honeycomb formation was negligible water showed that few microorganisms Composite
after 24 hours at temperatures below were present. and that microbial growth histamine' Honey-
Anti- (mg/1oo 9 combing'
26.7°C (80°F). but it increased as high- had not occurred in the presence of the Treatment biotics' tuna) score
er incubation temperatures were used antibiotics. Whole fish None 164 3.0
and was optimum at about 32.2°C
(90°F). At 43.3°C (110°F) and above. Discussion Fish eviscerated
and degilled None 75.6 3.5
disintegration of the fish tissue pre- To study the relationship between Fish eviscerated.
vented quantitative evaluation of honey- histamine formation and decomposition degilled and
separated between
combing. it was necessary to determine how much sections 2 and 3 Yes 1.62 3.5-4.0
Table 6 shows the rate of honeycomb- histamine was present initially in fresh ,Penicillin. 160 units/ml; tetracycline hydrocholoride.
ing at the optimum temperature. J2.2°C skipjack tuna. This study confirms pre- 0.1 mg/ml.
Sum of histamine
(90°F). Honeycombing proceeded with- vious observations that fresh scombroid 'Composite histamine = in all sections (mg) x 100.
out any apparent lag and increased grad- fish contain very little free histamine Total weight of
ually until 22.5 hours when appreciable (Geiger et aI., 1944; Hillig, 1956a; Fer- 'See Table 1
fish sections (g)

decomposition was noted. At 30 hours, encik,1970).

breakdown of the connective tissue was The effect of temperature on hista-
widespread. and at 37.5 hours destruc- mine formation in scombroid flsh has
tion was complete. been discussed in a number of publica-
tions (Kimata, 1961; Ienistea, 1973; Ed-
Effect of Antibiotics
munds and Eitenmiller, 1975; Arnold have an ample supply of live skipjack
Table 7 shows the effect of penicillin and Brown, 1975; Lerke et aI., 1978; tuna available for experiments. Hence,
and tetracycline on honeycombing and Fernandez-Salguero and Mackie, 1979) the entire postmortem thermal history
histamine formation in skipjack tuna but with little agreement on minimum, of each fish was known, and it was pos-
held at 35°C (95°Fj. When an intact maximum, and optimum temperatures. sible to study the effect of temperature
tish was incubated for 24 hours. ample Two major reasons for the inconsisten- under carefully controlled conditions.
histamine (164 mg/100 g) was formed cies are that different species of fish Our study shows that the optimum
and moderate honeycombing (score = were studied and that variations oc- temperature for histamine production
J.O) occurred. After removal of the gills curred in fish handling before incuba- in skipjack tuna is 37.SoC (lOOoF) and
and viscera. the histamine level was re- tion. In this study we were fortunate to that, as others have reported, the hista-

12 Marine Fisheries Review

mine is not uniformly distributed tive enzymes have been found in the Fernandez-Salguero. 1.. and I. M. Mackie. 1979.
Histidine metabolism in mackerel (Scomber
throughout the fish (Hillig, 1956a; lysosomes of other animals. it is tempt- scombms). Studies on histidine decarbox-
Ienistea, 1973; Lerke et aI., 1978). Inhi- ing to speculate that collagenolytic en- ylase activity and histamine formation during
bition by penicillin and tetracycline ob- zymes in the lysosomes of skipjack tuna storage of flesh and liver under sterile and
non-sterile conditions. 1. Food Technol.
served in this study also supports the may be responsible for honeycombing. 14:131-139.
widely held view that histidine decar- Considerable investigation would be Finch. R.. and G. Courtney. 1976. The tuna
boxylating bacteria are responsible for needed to identify these enzymes and to industry. In M. E. Stansby (editor). Industrial
fishery technology. p. 91- 109. Robert E.
the presence of histamine in scombroid determine their location. Moreover, it is Krieger Publ. Co.. Inc., Huntington. N.Y.
fish (Geiger et aI., 1944; Tomiyasu and possible that some of the proteolytic Geiger. E. 1944. Histamine content of unpro-
cessed and canned fish. A tentative method
Zenitani, 1957; Shifrine et aI., 1959; microorganisms present in scombroid for quantitative determination of spoilage.
Kimata, 1961; Ferencik, 1970; Ienistea, fish may contribute to honeycombing Food Res. 9:293-297.
1973; Edmunds and Eitenmiller, 1975; under natural conditions. Third, we _---,---__. 1948. On the mechanism of hista-
mine formation. Arch. Biochem. 17:391-395.
Taylor et aI., 1977; Arnold and Brown, have employed a quantitative scale to -----:_----,--:-. 1955. Role of histamine in poison-
1978; Omura et aI., 1978; Fernandez- evaluate honeycombing to compare the ing with spoiled fish. Science (Wash., D.C.)
Salguero and Mackie, 1979; Taylor et effect of different variables (e.g., tem- 121 :865-866.
-----:_ _:-::. G. Courtney, and G. Schnaken-
aI., 1979) and that histamine is not perature. time, etc.) on destruction of berg. 1944. The content and formation of
formed physiologically by fish tissue the connective tissue. We anticipate that histamine in fish muscle. Arch. Biochem.
3:311-319.
under aseptic conditions (Geiger et aI., changes can be made to improve the Griffiths. F. P. 1937. A review of the bacteri-
1944; Geiger, 1955; Ferencik, 1970; accuracy and usefulness of this scale for ology of fresh marine-fishery products. Food
Fernandez-Salguero and Mackie, 1979). skipjack tuna as well as other tuna that Res. 2:121-134.
Hardy. R., and 1. G. M. Smith. 1976. The stor-
The postmortem temperatures of de- are subject to honeycombing. age of mackerel (Scomber scombrusl. Devel-
composing scombroid fish usually are opment of histamine and rancidity. J. Sci.
moderate; hence, honeycombing and
Acknowledgments Food Agric. 27:595-599.
Hillig, F. 1954. Individual volatile acids. suc-
histamine formation generally develop This investigation was supported by cinic acid. and histamine as indices of de-
at slower- than-optimal rates under nor- Contract 03-6-208-35369 from the composition in Atlantic "little tuna" (Eu-
/hynnus aile/era/us). J. Assoc. Off. Agric.
mal conditions. Occasionally, however, National Marine Fisheries Service, Chern. 37:927-931.
fish temperatures can become high, par- NOAA. We thank Carlene M. Char and _ _--,----_. 1956a. Volatile acids. succinic acid.
ticularly in warm tropical waters and Pam K. Goto for their expert technical and histamine as indices of decomposition in
tuna. J. Assoc. Off. Agnc. Chern. 39.773-800.
during prolonged exposure on the hot assistance. _-,--__ . 1956b. Note on honeycombing in
deck of the fishing vessel. In these in- decomposed tuna. J. Assoc. Off. Agric.
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