Food Protection Trends - January/February 2021 - 39

et al. (51) tested for bacterial histamine formation at 0°C
in mackerel sections (Scomberomorus maculatus) and found
6 ppm after 10 days. Kerr et al. (39) tested for bacterial
histamine formation at 0°C in yellowfin tuna (Thunnus
albacares) and found 1 ppm after 4 days and 25 ppm after
8 days. To date, these are the lowest temperatures at which
histamine formation has been found, regardless of species of
fish or bacteria.
The list of histamine-forming bacteria that have been
reported to form histamine at ≤2°C and the relevant periods
of time is given in Table 1. All other reported histamineforming bacteria found need higher temperatures for
histamine formation. Table 1 includes some high histamine
parts per million for various conditions. Behling and Taylor
(6) reported ~143 ppm of histamine had formed after
6.5 days in tuna infusion broth at 0°C after starting with
a Klebsiella inoculum of 107 CFU/mL, which was several
orders of magnitude higher than the level expected on wild
fish. Emborg and Dalgaard (21) started with an inoculum of
M. psychrotolerans at 103 CFU/mL and obtained 100 ppm of
histamine in broth after 9 days at 1.7°C.
Although raw fish rapidly chilled and held on ice or in
refrigerated sea water at −1°C may allow some production
of histamine at very low concentrations over long periods of
time (40), this short-term control of histamine formation at
low temperatures is why boats using ice or refrigerated sea
water have been successful. At these temperatures, decomposition by odor-causing bacteria is the primary cause for
rejection of spoiled fish, not histamine concentrations. The
HACCP Guidance of 2011 (69) recommends organoleptic
evaluation of 118 fish per lot of tuna (max 25 mt) at receiving
for all deliveries. This evaluation identifies decomposition in
the fish from odor-causing bacteria. Every tuna packed under
U.S. federal inspection must be organoleptically evaluated by
trained factory workers, and federal inspectors must audit the
process continuously (59).
In summary, the decarboxylation of histidine to form
histamine is a very slow process at ≤ 0°C. The use of ambient
tempering room temperatures of −3 or −4°C (i.e., below the
temperature of the phase change from ice to water; latent
heat of fusion) will control the risk of histamine formation.
At the end of the tempering phase, the fish core should be −3
to −4°C, and this process will decrease the ensuing thawing
times in water to prepare the tuna for butchering, organoleptic inspection, and precooking.
Tuna Processing
A critical first phase in tuna processing is thawing the
frozen fish because tuna usually is delivered and stored
frozen. Previously frozen tuna and never frozen tuna require
very different processing to control histamine formation
(69); therefore, here we will assume that the tuna arrives at
the factory frozen or is frozen on arrival and that the factory
uses a precooking CCP as described in scenario 4.

Tuna are usually stored at −18 to −20°C; thus, thawing
starts with very cold fish. Extra time is required to thaw large
fish because may be needed to thaw them properly depending
on size, water temperature, and water circulation speed ( JDB,
personal communication). Results from thawing studies (3,
36) indicate that an increase in the water or air temperature
has more impact on thawing rates than does increasing the
speed of water or air circulation. If the initial temperatures
of large fish were increased prior to water thawing, they
could be thawed in less time. These considerations support
increasing the body temperature of the large tuna through
tempering before thawing.
During thawing, as the core temperature increases, the
consistency of the fish flesh changes from frozen very hard
to something less hard. When a fish starts with a very cold
initial temperature, more time is required for thawing than
when the fish starts with a higher core temperature ( JDB,
personal communication).
In this document we define the following terms for
increasing the temperature of frozen tuna: (i) thawing
happens in water or air at >4.4°C; (ii) tempering happens in
air at ambient temperatures of less than −3°C.
Tempering for frozen fish that will be precooked does not
involve holding at >4.4°C ambient air temperature for some
amount of time before turning on the thaw water because
at >4.4°C the initial 12-h CL for processing tuna starts. The
process we propose does not affect that initial 12-h limit.
Tempering times for large tuna may be ≥ 48 h. The
important aspect of using tempering as a CCP and CL
is maintaining the air temperature of the environment
throughout the tempering phase at below −3°C to control
histamine formation as the increase in fish core temperature
is occurring. In recent warning letters (66, 72), the FDA
suggested using a continuously recording thermometer
for monitoring thawing temperatures (air or water)
at temperatures <4.4°C (40°F) when thawing at that
temperature is a CL and/or CCP.
One of our coauthors (F.N.) used Time to Temper software
(Global Cold Chain Alliance, Arlington, VA) to estimate
tempering time for fish of different sizes. The parameters used
were an initial temperature of −18°C, an end point of −3°C,
and a moving air temperature of −3°C. The estimated number
of tempering hours by fish size are listed in Table 2. Each
factory will have to verify tempering times and temperatures
with their own equipment and operating conditions.
When the tuna precooking target CL of 60°C at the core
is not met and the batch must be recooked, the entire initial
time of the precooking cycle must be added to the 12-h thaw
and butcher time limit. If the 12-h CL is exceeded, then
necessary corrective actions are required (70).
In practice, U.S. tuna boats were tempering the fish in the
1950s, 1960s, and 1970s before unloading directly to the
canneries. At that time, the fish were packed very tightly in
the wells, and the fish had to be tempered so they could be

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