444

Journal of Food Protection, Vol. 81, No. 3, 2018, Pages 444–455

doi:10.4315/0362-028X.JFP-17-276
Published 2018 by the International Association for Food Protection
This is an open access article under the CC BY-NC-ND license (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Research Paper

Precooking as a Control for Histamine Formation during the

Processing of Tuna: An Industrial Process Validation
FARZANA ADAMS,1 FRED NOLTE,2 JAMES COLTON,3 JOHN DEBEER,4* AND LISA WEDDIG5

128 Langdale Court, Huntington, Hamilton 3210 New Zealand; 2Fred Nolte Consulting, 2503 West 5th Avenue, Vancouver, British Columbia, Canada

V6K 1S9; 3Aerojet Rocketdyne, 8900 De Soto Avenue, Canoga Park, California 91304, USA; 4Chicken of the Sea International, 2150 East Grand Avenue,

Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023

El Segundo, California 90245, USA; and 5National Fisheries Institute, 7918 Jones Branch Drive, #700, McLean, Virginia 22102, USA

MS 17-276: Received 16 July 2017/Accepted 7 November 2017/Published Online 23 February 2018

ABSTRACT
An experiment to validate the precooking of tuna as a control for histamine formation was carried out at a commercial tuna
factory in Fiji. Albacore tuna (Thunnus alalunga) were brought on board long-line catcher vessels alive, immediately chilled but
never frozen, and delivered to an on-shore facility within 3 to 13 days. These fish were then allowed to spoil at 25 to 308C for 21
to 25 h to induce high levels of histamine (.50 ppm), as a simulation of ‘‘worst-case’’ postharvest conditions, and subsequently
frozen. These spoiled fish later were thawed normally and then precooked at a commercial tuna processing facility to a target
maximum core temperature of 608C. These tuna were then held at ambient temperatures of 19 to 378C for up to 30 h, and
samples were collected every 6 h for histamine analysis. After precooking, no further histamine formation was observed for 12
to 18 h, indicating that a conservative minimum core temperature of 608C pauses subsequent histamine formation for 12 to 18 h.
Using the maximum core temperature of 608C provided a challenge study to validate a recommended minimum core
temperature of 608C, and 12 to 18 h was sufficient to convert precooked tuna into frozen loins or canned tuna. This industrial-
scale process validation study provides support at a high confidence level for the preventive histamine control associated with
precooking. This study was conducted with tuna deliberately allowed to spoil to induce high concentrations of histamine and
histamine-forming capacity and to fail standard organoleptic evaluations, and the critical limits for precooking were validated.
Thus, these limits can be used in a hazard analysis critical control point plan in which precooking is identified as a critical
control point.
Key words: Challenge study; End point internal product temperature (EPIPT); Histamine; Precooking; Tuna; Validation

The principles of hazard analysis and critical control
point (HACCP) plans (42) require the use of science-based
evidence to validate a preventive process control as capable
of effectively limiting an identified food hazard. The food
safety regulation for the production of seafood products
published by the U.S. Food and Drug Administration (FDA)
(38) is based upon HACCP principles. This article describes
an in-plant, full-production-scale validation process for
ascertaining that precooking tuna to a minimum core
temperature of 608C pauses histamine (scombrotoxin)
formation for at least 12 to 18 h, thus giving processors
enough time to process fish of any size.
All seafood sold for human consumption in the United
States must be processed according to the FDA’s seafood
HACCP regulation (21 CFR 123) (38). To facilitate
compliance, the FDA has provided extensive guidance to
the industry in the form of a document, ‘‘Fish and Fishery
Products Hazards and Controls Guidance’’ (42). This FDA
HACCP guidance provides the strategies, i.e., critical
control points (CCPs) and critical limits (CLs), for control
* Author for correspondence: Tel: 760-670-6141: Fax: 760-436-5178;
E-mail: john.debeer@thaiunion.com.
of various hazards associated with seafood products.
Alternative approaches for controlling hazards at CCPs
must be proven valid by the processor. The FDA seafood
HACCP regulations mandate that processors ‘‘verify that the
HACCP plan is adequate to control food safety hazards that
are reasonably likely to occur’’ (38).
Fast-moving scombroid fishes, such as tuna, tend to
have more free histidine in their muscles than do other
fishes; therefore, higher concentrations of histamine and
other amines can form (21, 32). Histamine will be formed in
these fish when they are not chilled properly after capture.
Histamine-forming bacteria (HFB) are ubiquitous in the
marine environment, and under unchilled conditions, HFB
in tuna can grow. The HFBs produce the enzyme histidine
decarboxylase (HDC), which converts free histidine within
the tuna muscle into histamine (3). Histamine is a relatively
small, very stable toxin and is not inactivated by cold or heat
(15).
Histamine and other amines are the primary cause of
scombrotoxin reactions, often called histamine poisoning
(18). Histamine poisoning is the leading cause of seafood-
borne illness in the United States and internationally (7, 14).
The defect action concentration for histamine in tuna flesh in
J. Food Prot., Vol. 81, No. 3
the United States is 50 ppm (37), and the toxic concentration
is 500 ppm (37).
No histamine is found in freshly caught tuna (16, 21),
but when these fish are not handled properly at sea,
histamine will form and accumulate. Chilling and/or
freezing the fish promptly after capture will prevent the
growth of HFB and histamine formation (42). The tuna
fishing vessels in all major fisheries either chill the tuna with
ice or refrigerated seawater (RSW) or freeze the tuna at sea
with a blast freezer or brine freezing system (6, 17). Diligent
time-temperature controls throughout the supply chain are
essential to assure consumer safety because tuna fishing and
processing are primarily done in the tropics, with typical
ambient temperatures that could potentially lead to spoiled
tuna with high histamine concentrations.
The basic method for tuna canning has been described
by Bell et al. (4) and DeBeer et al. (8). Tuna loins are the
desired tuna portions for canning. To facilitate skinning,
deboning, and separating the red meat from the loin meat,
the fish are initially heat treated in a process known as
precooking (8). Tuna processors sometimes inject vegetable
broth into the raw tuna loins to add flavor and improve
texture. This vegetable broth is a flavoring allowed in the
U.S. canned tuna standard of identity (40).
The FDA HACCP guidance (42) sets limits for the time
allowed for processing tuna to 12 h from the time the tuna
starts thawing until it has been sealed in cans and the retort
has started or the loins start to freeze, if the ambient
temperature exceeds 218C at any time. Procedures that must
be conducted in this time window include thawing,
precooking, cooling, removing the skin and bones, separat-
ing the red meat from the loins, and preparing the fish for
canning or freezing. This 12-h window is not sufficient for
thawing, precooking, and cooling larger tuna. However, the
HACCP guidance does allow an intermediate heat step when
processors can demonstrate that histamine formation can be
delayed long enough after precooking to allow additional
processing time, i.e., to ‘‘restart the clock’’ (8, 42). Although
most processors believe that precooking provides an
adequate process control for safely producing canned tuna
without elevated histamine concentrations, no scientific
studies have been conducted using the ‘‘worst-case’’
conditions to validate the use of precooking to restart the
clock (F.A., personal communication).
FDA warning letters (41, 43) and the subsequent
collaboration between the FDA and the National Fisheries
Institute identified a specific lack of data for demonstrating
the effect of precooking on controlling the formation of
histamine. One such warning letter (41), in October 2010,
stated there was no precooking step listed in the existing
HACCP plan as a CCP ‘‘to ensure control of exposures to
operations to control scombrotoxin formation.’’ The warning
letter went on to say, ‘‘the HACCP plan should include the
pre-cook as a critical control point and should include all
appropriate critical factors to achieve an adequate cook.’’
Therefore, precooking CCP and CL studies are clearly
needed.
Enache et al. (13) conducted thermal death time studies
on five species of known HFB (Morganella morganii,
Raoultella planticola, Hafnia alvei, Enterobacter aerogenes,
CONTROL OF HISTAMINE FORMATION BY PRECOOKING 445
and Photobacterium damselae) and found that M. morganii
was the most heat resistant; therefore, a heat treatment
designed to control M. morganii would effectively control
the other HFB. Nolte et al. (25) further developed a model
demonstrating that once the tuna reaches a core temperature
of 608C, M. morganii populations have undergone a
significant 5-log reduction. In other studies, the activity of
HDC produced by M. morganii was reduced by 56% at 508C
and by 99% at 608C (20). Osborne and Bremer (27) used the
Bigelow model to determine the thermal death times for M.
morganii in kahawai (Arripis trutta). That model indicated
that the minimum precooked core temperatures should be 58
to 628C to ensure that the final product would not produce
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
histamine during subsequent temperature abuse (5, 27). The
most common target end point internal product temperature
(EPIPT) for precooked tuna for the past 50 years (F.N.,
personal communication) has been a minimum meat
temperature at the backbone of 1358F (57.28C), as developed
by Peterson in 1971 (30).
The validation of a HACCP CL involves testing to
determine whether the CL can control the worst case of the
hazard. In this article, the worst case for tuna spoilage refers
to tuna that has been subjected to deliberate time-
temperature abuse to reach exponential histamine formation,
thereby providing practical evidence of HFB presence in the
test fish. The test fish also needed to fail standard
organoleptic evaluations and exceed the FDA guidelines
for histamine (50 ppm), thus indicating the presence of HFB.
The objectives of this study were to (i) precook worst-
case spoiled tuna to a target maximum core temperature of
608C to validate the precooking process as stopping or
pausing histamine formation and (ii) determine and validate
how much extra processing time is therefore gained from
precooking the tuna to a minimum core temperature of 608C
by sampling tuna at different periods after precooking to
determine whether histamine formation has been paused for
a significant period.
MATERIALS AND METHODS
Design of the validation experiment. After comprehensive
consultations with experts and statisticians from the FDA, a set of
validation experiments was designed to accomplish the two study
objectives. Tuna were to be brought on board the fishing vessels
alive, spoiled to obtain histamine concentrations higher than 50
ppm, and then precooked to a targeted maximum of no higher than
608C at the core to determine whether histamine formation could
be paused for sufficient time to process larger tuna (at least 12 to 18
h after precooking). For purposes of validation, fish were
deliberately spoiled before precooking to simulate time-tempera-
ture abuse on the catcher vessels and to satisfy the burden of proof
required under the FDA’s seafood HACCP regulation (38).
Fish capture. All the experimental albacore tuna (Thunnus
alalunga) were caught by longline fishing vessels near Fiji and
brought on board alive. Fish were immediately chilled on board in
ice or RSW and stored at 2 to 08C. The 226 albacore used in this
experiment had a mean weight of 15 kg each.
Fish spoilage. All fresh raw tuna were landed and then
spoiled in Suva, Fiji, on two separate days. The spoilage process
started immediately after the tuna were unloaded, and each fish
446 ADAMS ET AL.
TABLE 1. Design of experiment for the number of fish used for each treatment for the two precooker temperatures
Treatment group Fish type Injection Precooker temp (8C)
A Round No 70
B Round No 100
C Splitb No 70
D Split No 100
E Split Yes 70
F Split Yes 100
G Round No Not cooked (control)
a
Before-precook samples were collected from raw fish approximately 30 min prior to the start of precooking. Time 0 (T0) samples were
collected after precooking from both the raw fish and the precooked fish after precooked fish were removed from the precooker. The T12,
T18, T24, and T30 samples were collected 12, 18, 24, and 30 h after T0. Of the six fish replicates for T0 through T30, five had been
chilled in RSW and one had been chilled in ice onboard the harvest vessel. Differences were not expected, and these two chilling methods
were evenly stratified.
b
For all split fish, one-half of each fish was used as the raw control.
subsequently was spoiled to greater than 50 ppm of histamine.
During the spoilage process, the fish were stored in open fish bins
containing seawater for up to 25 h with temperatures that were
controlled at 25 to 338C. The method of deliberate spoilage of
these fish is described in the Supplemental Material. After spoilage,
the fish were completely frozen in air blast freezers (Dalian
Refrigeration Company, Dalian, People’s Republic of China) set at
408C and held for at least 24 h. The spoiled frozen fish were then
transferred by freezer truck (208C) to the processing facility.
Thawing and processing. All precooking experiments were
conducted in precookers (Leonard Engineering, El Cajon, CA) at a
commercial tuna processing facility in Levuka, Fiji. Two
precooking experiments were conducted each day for 3 days.
Standard methods for commercial tuna processing were used for
thawing and evisceration to prepare the fish for precooking. The
fish were thawed for 11 h to a target core temperature of 2 to 08C
in unchlorinated single-use seawater. The thawing water temper-
ature was approximately 26 to 288C. The thawed fish were
butchered by removing the stomach, liver, heart, and other entrails.
Some of the round fish were subsequently split. The heads and gills
were not removed from the round or split tuna; however, the heads
and gills were removed from the split injected fish. In this article,
round fish means unsplit tuna fish with the stomach, liver, heart,
and other entrails removed.
Fish preparation. In all, 226 fish and 1,112 individual
samples were used for histamine analysis to validate this
precooking procedure. The design of experiment (DOE) stipulated
six precooker treatment combinations (A through F) using 32 fish
each (Table 1). Six fish pieces were tested after precooking at each
of five sampling times for each treatment. Each fish piece was
uniquely identified throughout the entire processing cycle. This
DOE matrix of precooker treatments allowed for comparisons
among the factors: whole round fish, split fish, split fish injected
with vegetable broth (round fish were not injected for technical
reasons), and cooking at the two precooker target steam
temperatures (70 and 1008C).
Before precooking, the round fish (treatments A and B) were
placed directly into fish baskets, with one fish per basket, and then
into precooker racks. The round fish controls (treatment G), which
were raw (without precooking treatment), were also placed into
fish baskets and precooker racks in the same way so that these
J. Food Prot., Vol. 81, No. 3
No. of fisha
Before precook T0 T12 T18 T24 T30 Total
2 6 6 6 6 6 32
2 6 6 6 6 6 32
2 6 6 6 6 6 32
2 6 6 6 6 6 32
2 6 6 6 6 6 32
2 6 6 6 6 6 32
2 4 4 4 4 4 22
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
control fish could accompany the precooked fish throughout the
rest of the process after precooking.
The fish for the noninjected treatments C and D were split in
half using the butchering split saw and placed into fish baskets in
single layers (two pieces per basket), and the baskets were placed
into precooker racks. The fish for the split-injected treatments E
and F were split in half, injected with vegetable broth using
commercial injectors, and placed into fish baskets and fish racks in
a manner similar to that for the split noninjected tuna. One half of
each individual fish in the four split fish treatments (C, D, E, and F)
was precooked, and the other half served as an uncooked raw
control. The split fish halves were randomized such that the left or
right halves were randomly assigned to either the precooked or raw
control group. Therefore, the only difference between experimental
groups and the controls was the precooking heat treatment,
allowing for strong paired statistical analysis.
The fish from the two chilling methods aboard the longline
catcher vessels (ice and RSW) were evenly distributed across the
precooker treatments such that any potential differences could be
identified during the statistical analysis. Of the six fish for each
treatment sampling time, one had been chilled in ice and five had
been chilled in RSW.
Precooker target temperatures and validation. Commer-
cial precookers using direct contact steam were used to precook the
fish. Precooker temperatures of 70 and 1008C were selected to
bracket the range of steam temperatures used in commercial
precooking schedules. This design allowed for comparison of
potential differences resulting from precooking times and temper-
atures typically encountered in routine commercial procedures,
e.g., lower precooker chamber temperatures requiring longer
cooking times versus higher precooker chamber temperatures with
shorter cooking times (F.N., personal communication). Tempera-
ture distribution studies were conducted to verify a uniform
temperature distribution inside each precooker (F.N., personal
communication) (24). For each of the precooker treatments, the
precooker was filled with additional fish to replicate commercial
precooker operations and temperature distribution patterns. Ap-
proximately 6 metric tons of additional nontest fish were processed
per precooking treatment, for a total of 36 metric tons of nontest
fish or about 2,400 individual nontest fish.
Temperature monitoring. The core temperatures for all
precooked test fish and a sample of the nonprecooked control fish
J. Food Prot., Vol. 81, No. 3 CONTROL OF HISTAMINE FORMATION BY PRECOOKING
FIGURE 1. Sites on tuna from which samples were taken for
histamine analysis.
were monitored with standard thermal probes (type T thermocou-
ples, Omega Engineering, Norwalk, CT) connected to Calplex data
loggers (TechniCAL, Metairie, LA) (33). The temperatures of the
thawing water and sidespray were monitored every 30 min with
programmable MiniVACQ wireless temperature data loggers
(TMI-Orion, Castelnau-le-Lez, France) (34). Similarly, the ambient
air temperatures in the areas for thawing, preparation, sidespray,
conditioning, and packing were monitored with a MiniVACQ
recording device every 30 min. The probes were verified for
accuracy against a calibrated NIST traceable (National Institute of
Standards and Technology, Gaithersburg, MD) thermometer at 08C
(ice slurry), 1008C (boiling water), and 70 and 1008C set points
inside the precookers. The dial thermometers were calibrated
against an NIST traceable thermometer. Temperature data were
compiled and evaluated using Calsoft (TechniCAL), MiniVACQ
(TMI-Orion), and Excel (Microsoft, Redmond, WA) software.
Processing times. The frozen spoiled fish were thawed for 11
h, precooked for 2 to 5 h, and then cooled for 2 to 4 h in the
sidespray and conditioning rooms to reach core temperatures below
408C.
Raw fish controls. All raw fish controls, including the
uncooked halves of the fish from treatments C through F and the
round fish controls (G) for treatments A and B, were set aside in
the preparation area where the ambient temperature was 26 to 328C
while the test fish were being precooked. All uncooked raw fish
controls were treated in the same manner as the precooked fish
throughout the remaining steps of the process in the sidespray
cooling, conditioning, and packing rooms.
Precooking test fish. All test fish, except the raw controls,
were precooked as outlined in the experimental design (Table 1) to
a target precooker exit core temperature near but not exceeding
608C. Temperature probes connected to the Calplex data loggers
allowed close monitoring of fish core temperatures in real time
during precooking. Three free leads were also placed near the
precooker racks containing the precooked test fish to monitor the
precooker steam temperature at the top, middle, and bottom
positions of the rack.
As soon as the core temperature of any fish in the precooker
treatment approached the target of 608C, the steam was turned off,
and all fish, including the nontest fish, were removed from the
precooker as quickly and safely as possible. Fish core temperatures
447
were measured using dial thermometers and recorded immediately
for all 32 precooked test fish per treatment.
Sample collection time. For each treatment, six histamine
samples were collected after the core temperatures were recorded
(T0). The other precooked fish and uncooked raw controls were
moved immediately into the sidespray room, and cooling with a
water spray commenced to lower the precooked test fish core
temperatures to the range where histamine concentrations would be
expected to increase most rapidly (15). When the average core
temperature reached 458C, the fish were moved into the
conditioning room for a brief time. After the average precooked
fish core temperatures further cooled to 408C in the conditioning
room, the precooked and control fish were moved into the packing
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
room to challenge the tuna through exposure to ambient conditions
of 27 to 328C.
Samples for baseline histamine analysis before precooking,
designated B4PC, were collected from the raw fish controls and the
treatment fish approximately 30 min before precooking. After
precooking, histamine samples were collected from six fish per
treatment, plus the corresponding baseline control fish at each of
five sampling times: immediately (T0), 12 h (T12), 18 h (T18), 24
h (T24), and 30 h (T30).
Sample collection stratification. The precooking process
resulted in the desired maximum 608C exit core temperatures as
planned except in a few cases. The steam portion of the precooking
process was stopped before the core temperature of any fish in a
treatment reached 608C, but the fish core exit temperatures were
not collected until the fish had been removed from the precooker
(after 5 to 10 min). The core temperature continues to increase for a
time after the steam has been turned off due to residual heat
transfer or overshoot (8, 29). The 1008C precooker steam
treatments tended to have greater increases in fish core post-
precooking temperatures than did the 708C precooker steam
treatments because more residual heat remained within the outer
tissues of the fish cooked at higher temperatures. This limitation of
some fish having exit core temperatures higher than 608C was
addressed by selectively stratifying the fish across the five
sampling times. T0 was selected for the fish with the highest core
temperatures, because it was already known that the effect of fish
core temperature on the histamine concentration and its increase is
less important right after precooking than later. This selective
stratification was done to ensure that all the lower exit temperature
fish were sampled at the later sample times to determine the effect
of lower exit temperatures on histamine concentrations in
precooked fish over time. After stratification, the remaining fish
were randomized using fish core temperature results and sampled
across the five sampling times.
Sampling locations. Samples for histamine analysis (mini-
mum sample weight of 250 g) were collected from the following
locations on each fish piece (Fig. 1): (i) for round fish, anterior
dorsal and anterior ventral, right and left side, four samples per
fish; and (ii) for split fish, anterior dorsal, anterior ventral, and
middle ventral, three samples per split fish piece. Each sample
location on each fish can be tested only once because histamine
analysis is destructive. The anterior ventral location was chosen to
comply with the recommendations from the FDA HACCP
guidance regarding chemical testing for histamine (42), the anterior
dorsal location was chosen because of historical industry practices
based on research conducted by Frank et al. (16), and the middle
ventral sample location was suggested by the FDA experts for an
extra sample site on the split fish. Both the left and the right sides
448 ADAMS ET AL.
FIGURE 2. Histamine concentrations in tuna after spoilage
period in Suva, Fiji, and after thawing but before precooking in
Levuka, Fiji. A zero point was added based on the assumption of
zero histamine in freshly caught fish.
of all fish were sampled to further account for a possible
nonuniform distribution of histamine throughout the fish (12,
22). To preserve the samples for laboratory analysis, all samples
collected for histamine testing were immediately frozen using a
commercial plate freezer (19) and analyzed using the AOAC
fluorometric method 977.13 for testing histamine in seafood (1).
Sensory evaluations. Sensory evaluations were conducted by
sensory experts trained using the National Oceanic and Atmo-
spheric Administration and FDA sensory training protocols (36) on
each fish at the same time as samples were collected for histamine
testing.
DOE. The DOE was a three-factor full factorial repeated-
measures design with two treatments omitted (J.C., personal
communication) (23, 26) and a covariate. The factors are (i) round
and split, (ii) injection, and (iii) precooking steam temperature.
Sampling time after precooking (0, 12, 18, 24, and 30 h) was the
covariate. The DOE was for repeated measures (26) because each
fish piece was measured at three or four locations depending on
whether the fish was split or round (the three or four samples
collected per fish piece were analyzed at the same time).
Statistical analysis. The DOE called for equal numbers of
fish in each of the six precooking treatments. The histamine
concentrations were converted to natural logarithms (ln) for the
factorial analysis of variance (ANOVA) model statistical analysis.
The ln form reduces the impact of outliers and helps satisfy the
normality assumption for the ANOVA (J.C., personal communi-
cation).
The histamine results were analyzed with Minitab software
(State College, PA) and Microsoft Excel. The mean ln histamine
concentrations at each sampling time for each treatment group
were analyzed using a one-way ANOVA. The differences in the
histamine concentrations between the sampling times within a
treatment were evaluated using Tukey’s method for multiple
comparisons of means (35).
The ln histamine results also were analyzed with a regression
model to determine the comparative impacts of round versus split,
injection, precooker temperature, and sampling time after pre-
cooking. The terms were eliminated from the model with the main
effects and two-way interactions using a backwards elimination
approach of terms that were not statistically significant. A quadratic
J. Food Prot., Vol. 81, No. 3
term for sampling time was included to predict the time point when
the histamine concentrations would exceed the initial concentra-
tions.
RESULTS
Fish spoilage. The temperatures of the air, water, and
fish cores during fish spoilage are shown in Supplemental
Figure S1. The water temperature during spoilage was 25 to
328C, and fish core temperatures increased from less than
48C, when stored on ice or in RSW, to equilibration with
these ambient water temperatures during the 21- to 25-h
spoilage times (Fig. S1). Ten fish were tested for histamine
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
as indicators to stop the spoilage time. The histamine
concentrations were 66 to 214 ppm (Supplemental Table S1)
before freezing the rest of the intact fish. The fish were also
noticeably decomposed, as determined by sensory evalua-
tions. Subsequently, every fish tested throughout this study
had a histamine concentration higher than 50 ppm and had
odors of decomposition. The histamine concentrations at the
end of spoilage and after thawing but before precooking are
shown in Figure 2. An added data point of 0 ppm of
histamine based on historical data (16, 21) was included in
Figure 2 for reference to represent the lack of histamine in
the fresh fish at the start of spoilage.
Time-temperature exposure and precooking results.
The average core temperature profile for the precooked test
fish throughout the entire process is shown in Figure 3 and
includes the stages in order of progression: start of thawing,
end of thawing, precooker initial, precooker exit, cooling
during sidespray, and conditioning room. The ambient
temperatures in these processing areas were 25 to 358C
except in the conditioning room, which averaged 208C (Fig.
4). All ambient room temperatures were in the optimal
temperature zone for histamine formation (42).
EPIPTs. The resulting EPIPTs are charted in an
interval plot in Figure 5 and tallied in Table S2. The data
in Table S2 are grouped by degree and precooker treatment.
The target for the core precooker exit temperatures was
achieved: most fish had core temperatures lower than 608C,
and only 11% exceeded the target core temperature
maximum of 608C.
Histamine concentrations and statistical analysis.
The effects of fish core exit temperature, sampling time after
precooking, and the three analysis factors on the mean ln
histamine concentrations are shown in Table S3. Sampling
time (hours after precooking stopped) was the most
significant factor in predicting histamine concentrations in
precooked fish. The effect of sampling time on ln histamine
concentrations was nearly identical for the six treatments
studied (interval plot, Fig. 6). The core fish exit temperatures
were significantly associated with histamine concentrations
(t ¼ 4.97, P ¼ 0.000). For every 18C increase in the core
fish exit temperature, there was a 2.1% decrease in ln
histamine concentration at any time after precooking in these
high-histamine fish (Table S3).
J. Food Prot., Vol. 81, No. 3 CONTROL OF HISTAMINE FORMATION BY PRECOOKING
The differences in histamine concentrations over time
for the six treatment combinations versus the controls are
shown in Figure 7. The ANOVA results for raw versus
precooked fish are shown in Table S4 and were significant
(df ¼ 1, F ¼ 198.06, P ¼ 0.000).
The mean histamine concentrations (and standard
deviations) for all precooking treatment and sample time
combinations are shown in Table 2. The large standard
deviations indicate high variability in histamine concentra-
tions for particular treatment and sample time combinations.
An ANOVA was performed on each treatment group to test
for differences in mean histamine concentrations across
sampling times. Tukey’s multiple comparison method (35)
was used to identify which sampling times were significantly
different.
449
FIGURE 3. Mean fish core temperature
profile for the complete processing of test
fish: frozen, thawed, before precooking (PC
initial), after precooking (PC exit), during
sidespray (SS), and at exit from the chill
room (CR).
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
The ANOVA results (Table 2) with Tukey’s method
indicate that the mean histamine concentrations in the
precooked tuna at time points B4PC, T0, T12, and T18 were
not significantly different from the concentrations at
previous time points for any treatments. The mean histamine
concentration at T24 was significantly different from
concentrations at these earlier sampling times for treatments
B, D, and E. The mean histamine concentration at T30 was
significantly different from that at the earlier sampling times
for all treatments. In summary, no significant differences in
mean histamine concentrations were found until at least T24,
even in these severely spoiled and decomposed fish.
Based on calculations using the coefficients derived
from the regression model to fit a quadratic equation to the
data, on average the histamine concentrations started to
increase just after 18 h (18.7 h) after the fish were removed
FIGURE 4. Mean (line) and range (whis-
kers) of ambient temperatures in fish
processing areas.
450 ADAMS ET AL. J. Food Prot., Vol. 81, No. 3

FIGURE 5. Tuna core exit temperatures

(mean and 95% confidence interval) mea-
sured after precooking (70 or 1008 C) by
sampling time (0 to 30 h) and histamine
analysis treatment group: A, round fish,
708 C; B, round fish, 1008 C; C, split fish,
708 C; D, split fish, 1008 C; E, split fish
injected, 708 C; F, split fish injected, 1008 C.

Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023

FIGURE 6. Interval plot (mean ln and 95%
confidence interval) histamine concentra-
tions with by sampling time (0 to 30 h) and
treatment group: A, round fish, 708 C; B,
round fish, 1008 C; C, split fish, 708 C; D,
split fish, 1008 C; E, split fish injected, 708 C;
F, split fish injected, 1008 C.

FIGURE 7. Mean histamine concentra-

tions over time (0 to 30 h) in precooked
fish (solid lines) and raw controls (dashed
lines) by treatment group: A, round fish,
708 C; B, round fish, 1008 C; C, split fish,
708 C; D, split fish, 1008 C; E, split fish
injected, 708 C; F, split fish injected, 1008 C.
J. Food Prot., Vol. 81, No. 3 CONTROL OF HISTAMINE FORMATION BY PRECOOKING 451

TABLE 2. ANOVA results comparing histamine concentrations by sampling time within a precooking treatment
Histamine (ppm)

Raw control Precooked

Difference using
Treatment Time (h) n Mean SD n Mean SD Tukey’s means test

A: round fish, 708C Before precook 2 261 72 2 298 24 B

0 6 560 191 6 331 117 B
12 6 2,825 799 6 271 102 B
18 6 2,047 234 6 316 87 B
24 6 2,221 488 6 324 79 B
30 6 2,640 1,263 6 643 58 A
B: round fish, 1008C Before precook 2 261 72 2 286 84 B/C

Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023

0 6 560 191 6 310 82 C
12 6 2,825 799 6 290 85 C
18 6 2,047 234 6 247 102 C
24 6 2,221 488 6 348 50 B
30 6 2,640 1,263 6 533 140 A
C: split fish noninjected, 708C Before precook 2 294 50 2 292 53 B
0 6 353 59 6 247 43 B
12 6 725 181 6 294 44 B
18 6 758 268 6 275 39 B
24 6 2,181 565 6 343 47 B
30 6 2,015 324 6 548 290 A
D: split fish noninjected, 1008C Before precook 2 316 105 2 325 121 B/C
0 6 359 59 6 223 74 C
12 6 861 488 6 258 68 C
18 6 1,899 576 6 272 58 C
24 6 2,307 684 6 393 40 B
30 6 1,330 300 6 733 129 A
E: split fish injected, 708C Before precook 2 294 79 2 322 72 B/C
0 6 360 58 6 272 47 C
12 6 1,022 439 6 304 40 C
18 6 1,198 434 6 285 30 C
24 6 1,070 130 6 381 68 B
30 6 1,938 235 6 587 53 A
F: split fish injected, 1008C Before precook 2 227 43 2 283 20 B
0 6 385 121 6 253 31 B
12 6 478 152 6 255 31 B
18 6 857 94 6 259 47 B
24 6 1,712 448 6 315 48 B
30 6 1,700 356 6 594 126 A
All treatments combined Before precook 12 282 70 12 305 73 B/C
0 36 400 131 36 277 83 C
12 36 1,145 934 36 279 71 C
18 36 1,336 637 36 276 72 C
24 36 1,891 676 36 349 63 B
30 36 1,908 726 36 604 161 A

from the precooker. Figure 8 shows the quadratic function
(P ¼ 0.000).
High variability in histamine concentrations between
fish was observed throughout the study. Significant
differences in histamine concentrations were found between
individual fish treated identically (i.e., different fish ID
numbers; df ¼ 150, F ¼ 15.90, P ¼ 0.000) (Table S5). Three
or four sample locations were analyzed for histamine
concentrations for each piece of precooked fish, but because
the measurements within a single fish are correlated, these
samples are not independent. The repeated measures aspect
of this study was handled by analyzing the summary
statistics from each fish, i.e., the mean ln histamine
concentration. A second summary statistic, the maximum
ln histamine concentration, was also analyzed; these results
were essentially identical to those for the mean ln histamine
concentration.
Location effects. Significant differences in histamine
concentrations were found between sample locations on the
fish pieces (Table S5). The anterior dorsal location had the
lowest mean histamine concentrations, the anterior ventral
location had the next highest, and the middle ventral location
had the highest (df ¼ 2, F ¼ 32.83, P ¼ 0.000). This location
452 ADAMS ET AL.
FIGURE 8. Quadratic effect plot of mean
ln histamine concentrations versus time
after precooking (0 to 30 h). The quadratic
function becomes greater than T0 after
18.7 h.
effect was accounted for in the analysis by analyzing the
locations separately, and the results were essentially
identical to those obtained for the mean ln histamine
concentrations. No significant differences were found
between the left and the right sides of the fish (side factor
in Table S5).
Effects of chilling method. The method of chilling,
i.e., RSW or ice, was tracked throughout the study, but no
significant differences in histamine concentrations were
found for fish treated with these two onboard chilling
methods (df ¼ 1, F ¼ 1.043, P ¼ 0.311).
Effects of precooking temperatures. Two interactions
were significant: between round fish and precooker
temperature (df ¼ 1, F ¼ 7.14, P ¼ 0.008) and between
injected fish and precooker temperature (df ¼ 1, F ¼ 5.90, P
¼ 0.016) (Table S6). The precooker temperature for the
round 3 split interaction indicates that for round fish, the
higher precooker temperatures resulted in lower histamine
concentrations, whereas for the split fish, precooker
temperature did not have a significant impact on histamine
concentrations. The temperature 3 injection interaction
indicates that for split injected fish, the higher precooker
temperatures resulted in lower histamine concentrations. For
split noninjected fish, precooker temperature did not have a
significant impact on histamine concentrations. No interac-
tion was found between sampling time and any of the other
factors. Thus, although some significant interactions were
found between factors, no difference in the histamine
inhibiting effect of precooking was found under this
challenge study scenario.
DISCUSSION
The intent of this industrial precooking process
validation study was to validate the use of a precooker
EPIPT CL to control formation of histamine after precook-
ing. This study was conducted using fish with elevated
histamine concentrations and odors of decomposition.
Previous research indicated that 608C was an appropriate
J. Food Prot., Vol. 81, No. 3
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
target maximum EPIPT for this study. Precooking to this
target is a conservative CL and was used in this challenge
study with worst-case fish.
The fish used here had histamine concentrations that
exceeded the federal guidelines by 3- to 10-fold and were
thus considered beyond worst case. Although the design of
the spoilage portion of the experiment was to stop the
histamine formation at 50 ppm, because changes in bacterial
growth and histamine concentrations are variable and rapid
after 50 ppm of histamine is reached, the general spoilage,
bacterial growth, and increase in histamine concentration
cannot be stopped immediately (28, 31).
This validation challenge study was conducted with
freshly caught tuna that were live when caught and
histamine free. These fish were immediately chilled and
stored in ice or RSW until they were unloaded so the starting
histamine concentrations remained very low. It was
important that the fish not be frozen because freezing could
significantly reduce existing HFB populations. Therefore,
the subsequent spoilage process started with unfrozen fish of
excellent quality.
The water flow set up, temperature control, and air
circulation during the spoilage phase ensured that the water
temperature was in the range optimal for HFB growth and
histamine formation. The fish core temperatures rose from
safe temperatures of 2 to 08C to ambient temperatures close
to 328C, which are in the optimal range for HFB growth and
histamine formation (Fig. 2). The deliberate spoilage process
simulated a worst-case scenario of time-temperature abuse
that could occur on board a harvest vessel due to delays in
chilling and/or freezing of the fish. Resultant histamine
concentrations in the tuna exceeded the FDA defect action
level of 50 ppm (Table S1) on each spoiled experimental fish
tested by sampling at the end of spoilage or tested later as an
uncooked control.
The spoilage run was successful for creating fish with
histamine concentrations well in excess of 50 ppm.
Although the histamine concentrations at the end of the
spoilage period in Suva were 66 to 214 ppm, the histamine
concentrations of fish sampled before precooking at the
processing facility were 150 to 450 ppm. These histamine
J. Food Prot., Vol. 81, No. 3 CONTROL OF HISTAMINE FORMATION BY PRECOOKING
increases could have occurred at two processing steps, given
that the spoilage period had already successfully achieved a
high growth rate of HFB and histamine production could not
be immediately arrested (28, 31): (i) during the 1 h it took to
load the fish into the blast freezer and for the fish to be
frozen solidly (fish remained in the blast freezer for at least
24 h) and (ii) during the thawing phase (11 h in ~26 to 288C
seawater) because the HFB present were not destroyed by
freezing, transport, and storage. When thawed, the test fish
(those to be precooked and the uncooked controls) also had
strong odors of decomposition consistent with internation-
ally used evaluation standards (36). Thus, this validation
study was conducted with beyond worst-case frozen raw
material that would not normally be accepted by tuna
processors based on the CLs and sample sizes suggested by
the FDA HACCP guidance (42).
These fish with very high histamine concentrations were
precooked as described, and after precooking the fish core
temperatures were reduced to 458C in the sidespray room
and further to 408C in the conditioning room. The tuna only
spent between 2 and 4 h in the cooling zones to lower the
core temperatures, in contrast to general practices where
time in the cooling area is maximized and exposure to
ambient temperatures is minimized. These precooked high-
histamine decomposing fish were then further challenged by
exposure for up to 30 h to temperatures of 20 to 408C, which
are optimal for histamine formation (15).
The mean histamine concentrations and standard
deviations for all the treatments and sample times are shown
in Table 2. The large standard deviations indicate high
variability in these histamine concentrations, which is
consistent with the existing literature and is the reason for
the lower FDA action histamine concentration of 50 ppm
(31, 37).
In these experiments, precooking effectively stopped
histamine formation for up to 18 h after precooking in these
fish even though they had high initial histamine-forming
capacity before precooking, as indicated by the raw fish
control data. This histamine-forming capacity is a combi-
nation of both HFB and HDC, so both of these must have
been destroyed and/or denatured during precooking.
DeBeer et al. (9) found how much log lethality for HFB
is accumulated during extra minutes at core temperatures of
56 or 578C after precooking. According to Kanki et al.
(20), 99% of the HDC is inactivated at 608C. The target
goal of this project was to precook the fish core to no more
than 608C. Because the temperature at the core continues to
increase for some time after the steam is turned off (8, 29),
a core temperature of 608C means that the remaining
portions of the fish loin and red meat are also at higher
temperatures, effectively reducing the HFB levels or the
HDC activity, thus stopping the formation of histamine
until HFB growth resumes.
The large difference in histamine concentration between
the raw controls and the precooked fish (df ¼ 1, F ¼ 198.06,
P ¼ 0.000) (Table S4) also indicates that the short duration
of frozen storage did not affect the HFB and HDC (2) in the
uncooked control fish. There was some concern that the
freezing required to stabilize the tuna during transportation
from Suva to the processing facility in Levuka would
453
destroy the HFB, leading to protective effects and, thus,
compromising the study. Based on a limited number of
samples, Baranowski et al. (2) found that prolonged frozen
storage for 24 to 40 weeks was responsible for a reduction in
levels of surviving HFB in mahi-mahi (Coryphaena
hippurus). However, in the present study, the HFB in the
raw fish controls were not destroyed and were able to
produce high concentrations of histamine in the absence of
the precooking heat treatment; within 12 h, the concentration
increased two- to sixfold (Table 2). The short period of
frozen storage of less than 2 weeks in this study did not
curtail subsequent histamine formation.
The results of this study indicate that histamine
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
formation is delayed by precooking within the normal
ranges of steam temperatures in precookers, 70 to 1008C.
Consistent and significant differences in histamine concen-
trations were found between the raw fish controls and the
precooked fish treatments just after precooking and for a
significant period of time thereafter. These findings validate
the efficacy of precooking to control HFB levels and HDC
activity and, thus, curtail additional histamine formation and
accumulation for 12 to 18 h.
This precooking validation study was conducted with
fish that were beyond worst case: the minimum histamine
concentration recorded after thawing and before precooking
was 150 ppm (Fig. 2). No additional histamine formed until
18 h after precooking. The fish accepted by the tuna
processors have a maximum histamine level of 30 ppm,
which is five times lower than the minimum found in these
spoiled fish. Therefore, these results support a CL of 12 h
after precooking to control the formation of histamine with a
significant margin of safety (6 h) for deviation evaluations
(39). If a processor were to exceed the 12-h suggested time
limit, a prudent corrective action based on chapter 7 of the
HACCP guidance (42) could be used to determine the final
disposition of the fish. EPIPT sampling plans, minimum
sample sizes, and sampling strategies have been published
previously (10, 11).
The following conservative CLs, as part of a HACCP
plan built on a foundation of proper current good
manufacturing practices, sanitation standard operating
procedures, and prerequisite programs, will effectively
control the hazard of histamine during the production of
frozen tuna loins or canned products. These CLs are (i)
accepting fish with less than 30 ppm of histamine and
meeting sensory standards, (ii) controlling to less than 12 h
the time elapsed for processing the fish from the start of
thawing to the time precooker steam is turned on, (iii)
precooking the fish to a core temperature of at least 608C as
measured after fish are removed from the precooker (25),
and (iv) controlling to less than 12 h the time elapsed from
the end of precooking to the start of retorting cans or
freezing loins.
In conclusion, this experiment validated the process
used during the production of canned tuna or frozen tuna
loins of precooking the tuna to minimum core temperatures
of 608C to suppress the formation of histamine for 12 h or
longer after precooking.
454 ADAMS ET AL.
ACKNOWLEDGMENTS
This work was fully supported and funded by Bumble Bee Seafoods
and the Pacific Fishing Company. At the time these experiments were
conducted, F. Adams (née Munshi, formerly Vogl) and F. Nolte were
employees of Bumble Bee Seafoods and designed the experiments. F. Adams
was the primary scientist on the ground in Fiji. Roque Salazar, Gerald
Kontoh, Wayne Adams, and the plant operations team are gratefully
acknowledged for their assistance in carrying out the research work in Fiji.
Steven Mavity and Gina Ybanez (Bumble Bee Seafoods) are thanked for
their critical reading of experimental design, helpful discussions, and insight.
Scientists and statisticians from the U.S. FDA are acknowledged for their
substantive contributions into the study design. J. Colton (at Minitab at the
time of this research) coached the team on statistical design and data analysis.
Dr. Steve Otwell (retired professor, University of Florida, Gainesville) is
acknowledged for his subject matter expertise. Dr. Mona Baumgartel is
thanked for her editorial assistance. L. Weddig and J. DeBeer are members of
the National Fisheries Institute Canned Tuna Technical Committee and
facilitated the publication of this article. The authors thank the journal
reviewers for their very helpful suggestions to improve this manuscript. The
preliminary results of this body of research were presented at a fisheries
conference in 2012 (44) and have been used to validate the precooking CCP
in place in various canneries exporting canned tuna to the United States.
SUPPLEMENTAL MATERIAL
Supplemental material associated with this article can be
found online at: https://doi.org/10.4315/0362-028X.JFP-17-276.s1.
REFERENCES
1. AOAC International. 2012. Histamine in seafood. Official method
977.13. In Official methods of analysis, 19th ed. AOAC International,
Gaithersburg, MD.
2. Baranowski, J. D., H. A. Frank, P. A. Brust, M. Chongsiriwatana, and
R. J. Premaratne.1990. Decomposition and histamine content in mahi-
mahi (Coryphaena hippurus). J. Food. Prot. 53:217–222.
3. Behling, A. R., and S. L. Taylor. 1982. Bacterial histamine production
as a function of temperature and time of incubation. J. Food Sci.
47:1311–1314, 1317.
4. Bell, J. W., B. E. Farkas, S. A. Hale, and T. C. Lanier. 2001. Effect of
thermal treatment on moisture transport during transport during steam
cooking of skipjack tuna. J. Food Sci. 66:307–313.
5. Bremer, P. J., C. M. Osborne, R. A. Kemp, P. van Veghel, and G. C.
Fletcher. 1998. Thermal death times of Hafnia alvei cells in a model
suspension and in artificially contaminated hot-smoked kahawai
(Arripis trutta). J. Food Prot. 61:1047–1051.
6. Burns, F. D. 1985. Tuna handling and refrigeration on purse seiners.
NOAA technical memorandum. National Marine Fisheries Service.
Available at: http://docs.lib.noaa.gov/noaa_documents/NMFS/
SWFSC/TM_NMFS_SWFSC/NOAA-TM-NMFS-SWR-011.pdf. Ac-
cessed 2 April 2017.
7. Centers for Disease Control and Prevention. 2014. Surveillance for
foodborne disease outbreaks United States in 2012. Available at:
https://www.cdc.gov/foodsafety/pdfs/foodborne-disease-outbreaks-
annual-report-2012-508c.pdf. Accessed 7 July 2017.
8. DeBeer, J., F. Nolte, and C. W. Lord. 2015. Precooking tuna: a study
of the factors impacting the time required for precooking. Food Prot.
Trends 35:448–460.
9. DeBeer, J., F. Nolte, C. W. Lord, J. Colley, and L. Weddig. 2017.
Setting HACCP critical limits for the precooking CCP of commer-
cially processed tuna. Food Prot. Trends 37:176–188.
10. DeBeer, J., F. Nolte, C. W. Lord, J. Colton, and J. Colley. 2017.
Sampling plans to determine the minimum core temperature reached
during the precooking of tuna. Food Prot. Trends 37:269–288.
11. DeBeer, J., F. Nolte, C. W. Lord, J. Colton, J. Colley, and L. Weddig.
2017. A strategy for controlling histamine formation at tuna
precooking. Food Prot. Trends 37:340–352.
12. Edmunds, W. J., and R. R. Eitenmiller. 1975. Effect of storage time
and temperature on histamine content and histidine decarboxylase
activity of aquatic species. J. Food Sci. 40:516–519.
J. Food Prot., Vol. 81, No. 3
13. Enache, E., A. Kataoka, G. D. Black, L. Weddig, M. Hayman, and K.
Bjornsdottir-Butler. 2013. Heat resistance of histamine-producing
bacteria in irradiated tuna loins. J. Food Prot. 76:1608–1614.
14. Feng, C., S. Teuber, and M. E. Gershwin. 2016. Histamine
(scombroid) fish poisoning: a comprehensive review. Clin. Rev.
Allerg. Immunol. 50:64–69.
15. Food and Agriculture Organization of the United Nations, World
Health Organization. 2012. Public health risks of histamine and other
biogenic amines from fish and fishery products. Available at: http://
www.fao.org/fileadmin/user_upload/agns/news_events/Histamine_
Final_Report.pdf. Accessed 8 July 2017.
16. Frank, H. A., D. H. Yoshinaga, and W. Nip. 1981. Histamine
formation and honeycombing during decomposition of skipjack tuna
(Katsuwonus pelamis) at elevated temperatures. Mar. Fish. Rev. 43:9–
14.
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
17. Hamilton, A., A. Lewis, M. McCoy, E. Havice, and L. Campling.
2011. Market and industry dynamics in the global tuna supply chain.
Forum Fisheries Agency, Honiara, Solomon Islands. Available at:
https://www.ffa.int/node/567. Accessed 9 February 2017.
18. Hungerford, J. M. 2010. Scombroid poisoning: a review. Toxicon
56:231–243.
19. James, C., G. Purnell, and S. J. James. 2015. A review of novel and
innovative food freezing technologies. Food Bioprocess Technol.
8:1616–1634.
20. Kanki, M., T. Yoda, T. Tsukamoto, and E. Baba. 2007. Histidine
decarboxylases and their role in accumulation of histamine in tuna
and dried saury. Appl. Environ. Microbiol. 73:1467–1473.
21. Kim, S. H., H. An, and R. J. Price. 1999. Histamine formation and
bacterial spoilage of albacore harvested off the U.S. northwest coast.
J. Food Sci. 62:340–343.
22. Lerke, P. A., S. B. Werner, S. L Taylor, and L. S. Guthertz. 1978.
Scombroid poisoning. West. J. Med. 129:381–386.
23. Montgomery, D. C. 2004. Design and analysis of experiments, 6th ed.
Wiley, New York.
24. National Fisheries Institute. 2015. Canned tuna HACCP. Available at:
https://www.aboutseafood.com/about/about-nfi/canned-tuna-haccp.
Accessed 25 January 2017.
25. Nolte, F., D. G. Black, J. DeBeer, and E. Enache. 2014. Use of end-
point internal product temperature to control histamine formation in
tuna at pre-cooking step. Food Prot. Trends 34:94–100.
26. Oehlert, G. W. 2010. A first course in design and analysis of
experiments. Available at: http://users.stat.umn.edu/~gary/book/
fcdae.pdf. Accessed 22 March 2017.
27. Osborne, C. M., and P. J. Bremer. 2000. Application of the Bigelow
(z-value) model and histamine detection to determine time and
temperature required to eliminate Morganella morganii from seafood.
J. Food Prot. 63:277–280.
28. Patterson, P., and F. D. Burns. 1984. Salt uptake, and histamine and
honeycomb formation in brine frozen tuna. U.S. Tuna Foundation
technical report. Available at: john.debeer@thaiunion.com.
29. Pérez-Martı́n, R. I., J. R. Banga, M. C. Sotelo, S. P. Aubourg, and J.
M. Gallardo. 1989. Prediction of precooking times for albacore
(Thunnus alalunga) by computer simulation. J. Food Eng. 10:83–95.
30. Peterson, E. W. July 1971. Multipurpose cooker method. U.S. patent
3,594,196.
31. Staruszkiewicz, W. F., J. D. Barnett, P. L Rogers, R. A Benner, L. L
Wong, and J. Cook. 2004. Effects of on-board and dockside handling
on the formation of biogenic amines in mahi-mahi (Coryphaena
hippurus), skipjack (Katsuwonus pelamis) and yellowfin tuna
(Thunnus albacores). J. Food Prot. 67:134–141.
32. Taylor, S. L. 1986. Histamine food poisoning: toxicology and clinical
aspects. Crit. Rev. Toxicol. 17:91–128.
33. TechniCAL. 2014. CALPlex Datalogger. TechniCAL—the thermal
process authority. Available at: https://tcal.com/calplex-standard.
Accessed 14 April 2017.
34. TMI-Orion. 2015. MiniVACQ. Available at: http://www.tmi-orion.
com/en/data-logger-measure/temperature-data-logger/minivacq-
thermal-validation.htm. Accessed 14 April 2017.
35. Tukey, J. W. 1949. Comparing individual means in the analysis of
variance. Biometrics 5:99–114.
J. Food Prot., Vol. 81, No. 3 CONTROL OF HISTAMINE FORMATION BY PRECOOKING
36. University of Florida, Professional Seafood Sensory School. n.d. Mr.
James Barnett. Available at: http://www.daotao.vasep.com.vn/
Uploads/image/Nguyen-Ngoc-Dung/file/E_James%20Barnett.pdf.
Accessed 11 February 2017.
37. U.S. Food and Drug Administration. 1981. CPG Sec. 540.525.
Decomposition and histamine. Raw, frozen tuna and mahi-mahi;
canned tuna; and related species. Available at: http://www.fda.gov/
ICECI/ComplianceManuals/CompliancePolicyGuidanceManual/
ucm074506.htm. Accessed 24 December 2016.
38. U.S. Food and Drug Administration. 1995. 21 CFR 123. Fish and
fishery products. Fed. Regist. 60(242). Available at: https://www.
accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.
cfm?CFRPart¼123. Accessed 8 July 2017.
39. U.S. Food and Drug Administration. 1995. 21 CFR 123.7. Fish and
fishery products. Corrective actions. Available at: https://www.
accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.
cfm?fr¼123.7. Accessed 13 May 2017.
40. U.S. Food and Drug Administration. 2001. 21 CFR 161.190. Canned
tuna. Available at: https://www.gpo.gov/fdsys/pkg/CFR-2002-title21-
vol2/pdf/CFR-2002-title21-vol2-sec161-190.pdf. Accessed 24 March
2017.
455
41. U.S. Food and Drug Administration. 2010. Warning letter to Pacific
Fishing Company, 20 October 2010. Available at: https://www.fda.
gov/ICECI/EnforcementActions/WarningLetters/ucm262239.htm.
Accessed 26 February 2017.
42. U.S. Food and Drug Administration. 2011. Fish and fishery products
hazards and controls guide. Available at: http://www.fda.gov/
downloads/Food/GuidanceRegulation/UCM251970.pdf. Accessed
25 January 2017.
43. U.S. Food and Drug Administration. 2011. Warning letter to
Starkist, 1 March 2011. Available at: http://webcache.
googleusercontent.com/search?q¼cache:xcU5febrRyoJ:www.fda.
gov/ICECI/EnforcementActions/WarningLetters/2011/ucm245297.
htm&num¼1&hl¼en&gl¼us&strip¼0&vwsrc¼0. Accessed 9 April
2017.
Downloaded from http://meridian.allenpress.com/jfp/article-pdf/81/3/444/1692253/0362-028x_jfp-17-276.pdf by Malaysia user on 26 January 2023
44. Vogl, F., R. Salazar, F. Nolte, G. Kontoh, and G. Ybanez. 2012.
Validation for precooking as a control for potential histamine
production in tuna loins for subsequent canning. Presented at TAFT
2012, Proceedings of the 4th Trans-Atlantic Fisheries Technology
Conference, Clearwater Beach, FL, 30 October to 2 November 2012.