Research of relevance to histamine poisoning in New Zealand A review MAF Technical Paper No: 2011/70 Prepared for the Ministry of Agriculture and Forestry by Graham C Fletcher, Plant & Food Research, Mt Albert ISBN 978-0-478-38709-4 (online) ISSN 2230-2794 (online) July 2010
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Research of relevance to histamine poisoning in New Zealand
A review MAF Technical Paper No: 2011/70 Prepared for the Ministry of Agriculture and Forestry by Graham C Fletcher, Plant & Food Research, Mt Albert ISBN 978-0-478-38709-4 (online) ISSN 2230-2794 (online) July 2010
3.1.1 Histidine levels in whole New Zealand fish of various species 5 3.1.2 Levels of histamine and histamine-producing bacteria in hot-smoked fish 5
3.2 Bacterial growth and histamine production in whole kahawai 6 3.3 Thermal death 6
3.3.1 Hafnia alvei 6 3.3.2 Morganella morganii 7
3.4 Unpublished New Zealand research 8 3.4.1 Identification of histamine-producing bacteria in hot-smoked fish 8 3.4.2 Growth of individual bacterial strains in broth 9
3.5 Conclusions and industry recommendations 16
4 Literature update 2000–10 17 4.1 Other reviews 17 4.2 Methods 18
4.2.1 Extracting biogenic amines from seafood 18 4.2.2 Measuring histamine and other biogenic amines 18 4.2.3 Bacterial methods 20 4.2.4 Methods to determine fish species involved 21
4.3 Bacteria responsible 21 4.4 Products and handling practice effects 25 4.5 Time temperature considerations 28 4.6 Controls 30
4.6.1 Rapid refrigeration 30 4.6.2 Heading, gutting and skinning 31 4.6.3 Heat processing 31 4.6.4 Smoked and salted fish 31 4.6.5 Modified atmosphere packaging 32 4.6.6 Freezing and chilled storage 33 4.6.7 Gamma irradiation 33 4.6.8 Additives 33 4.6.9 Protective cultures of bacteria 34
4.7 Applying predictive models 34
5 Conclusions and recommendations 35
6 References 37
4366 July 2010 Research review: histamine poisoning in fish Page i
Executive summary Research of relevance to histamine poisoning in New Zealand – A review
Graham C Fletcher, July 2010, SPTS No. 4366
The context
Histamine poisoning from pelagic (predominantly scombroid) fish is a worldwide problem and in
many countries is the most common cause of food poisoning from finfish. It occurs when
bacteria convert high levels of naturally occurring histidine into histamine and, although the full
aetiology is not resolved, when people eat fish containing high levels of histamine they suffer
allergic type reactions. In New Zealand, histamine poisoning usually occurs after the
consumption of hot-smoked fish, and many of the outbreaks and recalls arise from the
consumption of local kahawai species. The author of the current report was part of a New
Zealand team that published a series of studies on this issue in the late 1990s including a set of
guidelines for the safe preparation of hot-smoked fish which were promulgated to industry.
However, there have been ongoing subsequent histamine poisoning outbreaks due to New
Zealand seafood, particularly hot smoked fish. The New Zealand Food Safety Authority
therefore requested that the findings of the New Zealand research be summarised and
subsequent international research be reviewed in order to identify future research or regulatory
actions that could help ensure the safety of New Zealand seafood.
Aim and research method
This report reviews published New Zealand work related to histamine production in New
Zealand fish carried out up to the year 2000. The results of unpublished work carried out by The
New Zealand Institute for Crop & Food Research on identifying the bacteria involved and
quantifying their growth and histamine production rates at different temperatures (0–20°C) are
also presented. Over 200 international research studies of relevance to the problem of
histamine have been published between 2000 and 2010 and this literature is reviewed from a
New Zealand perspective.
Review results
Previous New Zealand studies have determined the levels of histamine and its precursor,
histidine in retailed fresh and smoked fish products sold on the New Zealand retail market.
Studies have also assessed the growth of histamine producing bacteria and the development of
histamine in fresh and smoked kahawai. Subsequent international studies have broadened the
range of products identified as hazards for histamine production and particular advances
include understanding the role of histamine-producing bacteria able to grow at refrigeration
temperatures (psychrotrophic organisms) and the development of mathematical models to
describe the growth and histamine production of histamine-producing bacteria. Methods for
detection of histamine and for identifying histamine producing bacteria have been advanced and
a number of potential controls have also been investigated although some of these such as
irradiation are not applicable to New Zealand.
Recommendations
Recommendations from the review include:
Page ii 4366 July 2010 Research review: histamine poisoning in fish
1. Agencies investigating food-borne outbreaks of histamine poisoning should carry out
more detailed investigations: where possible remains of the actual implicated product
should be tested and laboratories commissioned to determine the species of fish
involved, to isolated and identify the bacteria involved and to determine the levels of
histamine and other biogenic amines present. Results of such investigations would
provide a clearer picture of the factors contributing to outbreaks of histamine poisoning
in New Zealand and help guide the development of methods to prevent such outbreaks.
2. The list of imported fish species that might be of food safety concern in New Zealand
should be revised to include species recently implicated in outbreaks overseas. This will
provide a warning to those handling such species to take extra care to prevent
histamine poisoning from them.
3. Analytical methods to quantify histamine and other biogenic amines should be reviewed
and implemented so that analyses of samples from New Zealand outbreaks can
contribute to the understanding of the aetiology of histamine poisoning.
4. Currently unpublished work on growth and histamine production by individual strains of
histamine producing bacteria should be published in an international peer-reviewed
journal to make the knowledge obtained available to international researchers and to
provide information to those developing mathematical models and software packages to
predict histamine formation.
5. The contribution of psychrotrophic bacteria to histamine production in fresh fish in the
New Zealand environment/context should be evaluated to determine whether these
contribute to the hazard and whether different handling and control guidelines are
required to protect against the hazard.
6. Histamine production in kahawai from the point of capture, including time spent in gill
nets should be investigated to determine the extent to which this presents a hazard and
whether new controls are needed for this aspect.
7. Methods should be developed and validated to evaluate the quality of at-risk fish
species so that fish that has been stored for too long can be identified and not be used
for hot smoking.
8. Factors that allow fish to develop problematic levels of histamine whilst appearing to be
safe to consume from a sensory perspective should be studied to understand whether
other methods of identifying hazardous fish need to be applied.
For further information please contact:
Graham C Fletcher The New Zealand Institute for Plant & Food Research Ltd Plant & Food Research Mt Albert Private Bag 92 169 Auckland Mail Centre Auckland 1142 NEW ZEALAND Tel: +64-9-926 3512 Fax: +64-9-925 7001 Email: [email protected]
4366 July 2010 Research review: histamine poisoning in fish Page 1
1 Introduction
Histamine (or scombroid) poisoning in humans is an intoxication that results from the
consumption of spoiled fish. The poisoning is only associated with a few fish species that
naturally contain high levels of histidine, the best known internationally being members of the
Scombridae family, particularly tuna and mackerel. Although the full aetiology of the intoxication
has not been resolved it involves high levels of histamine generated by spoilage bacteria
through the decarboxylation of histidine that naturally occurs at high levels in such species. The
toxin involved in the poisoning is known as scombrotoxin even though non-scombroid fish
species can cause the intoxication. A range of bacteria are capable of converting histidine to
histamine in fish. It has usually been attributed to bacteria which will only grow poorly if at all
below 10°C (mesophilic bacteria) such as Morganella morganii although some psychrotrophic
organisms which grow well at refrigeration temperatures such as Morganella psychrotolerans
have also been implicated. The symptoms resemble an allergic attack and, although usually
short-lived, are very unpleasant for those affected. In New Zealand, the illness has usually been
associated with hot-smoked fish of various species, particularly kahawai (Arripis trutta), not a
Scombridae fish.
Product recalls arising from histamine poisoning create a negative image for seafood products.
Although, histamine poisoning is usually caused by fish containing over 1000 mg/kg histamine,
incidents have been reported when levels as low as 200 mg/kg were detected (Bartholomew et
al. 1987). Outbreaks usually involve fewer than 10 people (Hughes et al. 2007) and often single
cases occur. The latter do not appear in statistics for food-borne outbreaks as, by definition, an
outbreak requires at least two people to be affected. Food safety is regulated by limiting the
amount of histamine permitted in fish flesh with the Australia/New Zealand food standard
requiring less than 200 mg/kg histamine (Australian and New Zealand Food Authority (ANZFA)
2010) while the US FDA has a hazard action level of 500 mg/kg and a decomposition level of 50
mg/kg (Food and Drug Administration 1995). The EC has a sampling plan based on 9 samples
requiring that no more than 2 exceed 100 mg/kg and none exceed 200 mg/kg although single
samples are allowed at the retail level (Commission of the European Communities 2005). The
draft Codex Alimentarius decomposition standard for smoked fish requires that product of
susceptible species not contain more than 100 mg of histamine per kg fish flesh although when
considering hygiene and handling the level is 200 mg/kg (Joint FAO/WHO Food Standards
Programme Codex Alimentarius Commission 2010). Despite the New Zealand standard being
200 mg/kg for food safety, New Zealand exported product must be able to meet the most
stringent standards of the world which is the FDA decomposition standard of 50 mg/kg so we
usually use this as the target in our research. The main way to ensure that susceptible product
remains within the prescribed limits is to store it at temperatures below the minimum for growth
of the mesophilic bacteria responsible for the histamine production or for durations such that
psychrotrophic bacteria do not have time to proliferate and produce unacceptable levels of
histamine.
From 1988 to 2000, the author was involved in a series of research projects designed to identify
practices that might mitigate the risks from New Zealand seafood. Although industry guidelines
were produced (Fletcher 1998a), New Zealand seafood has continued to cause outbreaks of
histamine poisoning up to the present. The New Zealand Food Safety Authority therefore asked
the author to review existing knowledge and make recommendations for future research.
The current report briefly reviews the New Zealand research that was carried out up to 2000,
presents some work that was hitherto unpublished and then reviews international research on
Page 2 4366 July 2010 Research review: histamine poisoning in fish
histamine poisoning between 2000 and 2010. The report makes some recommendations about
information that should be gathered in the event of any further outbreaks. It also presents the
case for a range of research projects designed to enhance our understanding of the factors that
lead to histamine poisoning and ways to reduce food safety risks. Information generated would
inform future management practices by the New Zealand seafood industry and guide policy and
planning activities in relevant regulatory agencies.
4366 July 2010 Research review: histamine poisoning in fish Page 3
2 Histamine poisoning in New Zealand
Before 2000, there were at least 27 published outbreaks of histamine poisoning in New Zealand
from New Zealand seafood. Early New Zealand publications detailing implicated products,
season and histamine levels included those by Foo (1975b) (canned mackerel and smoked
trevally (1), unspecified smoked fish (5). There was another well publicised outbreak from
smoked kahawai resulting in a recall of a batch of product produced from one smokehouse in
1997 (Anon. 1997). The dominance of smoked fish as the main product causing New Zealand
cases of histamine poisoning was unusual in the world and led to our research group, then part
of the DSIR, to initiate a research programme on controlling histamine poisoning from hot-
smoked kahawai as outlined in Section 3 of this report. Based on the work on kahawai, a
generic set of guidelines for the safe production of hot-smoked fish was produced (Fletcher et
al. 1998a) and distributed to every registered facility producing hot-smoked fish in New Zealand
but outbreaks have continued to occur (Table 1).
Information about New Zealand cases and outbreaks for the years 2006–09 is available on the
NZFSA website (Pirie et al. 2008; Williman et al. 2008; Williman et al. 2009; Lim et al. 2010).
This information has been supplemented with personal communications from Esther Lim, ESR
(2010) to produce a summary of the 31 reported outbreaks from 2000 to 2009 presented in
Table 1. During this period there have also been two major recalls in New Zealand, both from
hot-smoked kahawai produced by the same company (New Zealand Food Safety Authority
2002, 2003). This company has since ceased to trade.
In contrast to the rest of the world where fresh fish are the main cause of histamine poisoning
outbreaks, New Zealand outbreaks and product recalls are dominated by hot-smoked fish,
mostly kahawai (the only New Zealand product for which significant product recalls have been
required), but also marlin, trevally, kingfish, Spanish mackerel and tuna. Fresh or marinated
kingfish have also caused outbreaks of histamine poisoning in New Zealand as have fresh tuna
and marlin, canned mackerels and fish cakes (Table 1). The ongoing occurrence of outbreaks
from hot smoked fish points to the need for more research and/or tighter control of production
practices for hot-smoked fish by regulatory agents.
Page 4 4366 July 2010 Research review: histamine poisoning in fish
Table 1. New Zealand food-associated histamine poisoning outbreaks, 2006–09 (data extracted from Pirie et al. 2008; Williman et al. 2008; Williman et al. 2009; Lim 2010; Lim et al. 2010).
Year Month Location Product Setting Number ill *
2000 November Auckland Smoked fish Home, Seafood outlet 2P
2001 February Auckland Smoked fish Home 3P
2001 March Auckland Smoked fish (kahawai)
Home 2P
2001 August Auckland Smoked fish Home 2P
2002 January Auckland Smoked kahawai Home, Supermarket, Fish processor
2P
2002 January Auckland Smoked fish Home, Supermarket, Fish processor
5P
2002 January Auckland Smoked trevally Home, Fish processor 2P
2002 March Auckland, Tauranga
Smoked kahawai Home, Supermarket, Fish processor
3P
2002 December Auckland, Taupo, Waikato
Smoked kahawai Fish processor 16C, 4P
2003 March Auckland Smoked kingfish Fish shop 2C
2003 May Auckland, Waikato, Tauranga, Manawatu
Smoked kahawai Other food outlet 6C, 7P
2003 December Auckland Smoked kahawai Other food outlet 2C
2003 December Northland, Tauranga, Wanganui
Smoked kahawai Home, other food outlet 1C, 6P
2003 December Auckland Smoked kahawai Home, Seafood outlet 2C
2004 February Auckland Smoked kingfish Takeaway 2P
2004 March Auckland, Tauranga, Taranaki
Smoked kahawai Home, other food outlet 7C, 4P
2004 March South Canterbury
Smoked tuna Takeaway 2P
2004 April Auckland Smoked trevally Takeaway 2C
2004 May Auckland Marinated kingfish Home, other food outlet 2P
2005 March Auckland Smoked fish Home 2P
2005 May Auckland Smoked tuna Fish market 2C
2005 July Auckland Tuna steaks Restaurant/café 3P
2006 January Auckland Smoked tuna Home, Takeaway 2P
mackerel (Yung-Hsiang et al. 2005a), salted roe (Hsien-Feng et al. 2008), missoltini (salted air
Page 28 4366 July 2010 Research review: histamine poisoning in fish
dried twaite shad, Alosa agone) (Pirani et al. 2010), budu (a Malaysian fermented mixture of
anchovies and salt) (Rosma et al. 2009), (Egyptian salted-fermented fish) (Rabie et al. 2009),
fermented smoked fish (Petaja et al. 2000), Myeolchi-jeot (a Korean salted fermented fish
product) (Jae-Hyung et al. 2002), dried fish (Hsiu-Hua et al. 2009), fish dumplings (Hwi-Chang
et al. 2008), fish sauce (Poonsap 2000; Kimura et al. 2001; Jiang et al. 2010), fish-nukazuke (a
Japanese salted and fermented fish with rice-bran) and Indonesian lawa teri (fresh anchovy
mixed with citrus juice or vinegar and fried coconut) (Mahendradatta 2003). Korean smoked and
seasoned-dried Pacific saury (Cololabis saira) developed histamine levels of 120 mg/kg after 80
days at 19±5°C (Yong-Jun et al. 2001). Although not usually commercially produced in New
Zealand, any of these products may be imported for local ethnic communities and importers
need to be aware of the potential for histamine poisoning from such products. Ethnic
communities may also start producing these types of products from New Zealand raw materials
with potential for histamine formation. Dalgaard et al. (2008) made the point that many of these
products are strongly flavoured so are usually only consumed in small quantities, which may
explain the low level of food poisoning history attributed to them. An outbreak attributed to
salted milkfish did occur in 2006 (Yung-Hsiang et al. 2006). Working in China, Jiang et al.
(2010) found histamine levels ranging between 14 and 8400 mg/kg in fish sauces. This may be
of concern as imported fish sauces are commonly used in Asian cooking in New Zealand but
again, only small quantities are usually consumed.
In contrast to the products just mentioned, histamine levels were reported not to exceed 50
mg/kg in salted tuna roe (Periago et al. 2003). Although histamine-producing bacteria increased
during the salting process and some histamine formed during the first week of storage at 30°C,
properly stored salted tuna roe was not considered a serious health risk (Periago et al. 2003).
Similarly, while levels of histamine increased during the ripening of salted anchovies they did
not exceed 20 mg/kg (Pons-Sanchez-Cascado et al. 2005b). However, Australia recently had a
product recall due to histamine in dried whole anchovies imported from Vietnam (Food
Standards Australia New Zealand 2009).
Although there is speculation that biogenic amines form precursors for carcinogenic N-
nitrosamines in salted and dried fish (Al-Bulushi et al. 2009), these were not produced from
histamine in situ during heating with nitrites in a traditional Korean fermented anchovy dish (Jae-
Hyung et al. 2005). However, N-nitrosamines were produced from other biogenic amines
(putrescine and spermidine) (Jae-Hyung et al. 2005).
4.5 Time temperature considerations
The development of histamine is dependent on both storage time and temperature, with shorter
times being required at higher temperatures to reach a particular level of histamine. In
experiments, the formation of unacceptable levels of histamine has traditionally been associated
with storing product at unacceptably high temperatures for relatively long periods. For example,
Korean amberjack, mackerel, saury and Spanish mackerel did not show increases of histamine
until after 2 days’ storage at 7 or 10°C while little or no increases were observed during 7 or 9
days at 4°C (Min-Ki et al. 2009). Similarly tuna did not exceed 50 mg/kg histamine after a whole
day at 10 or 22°C (Du et al. 2002) or 6 h at 30°C (Jeya Shakila et al. 2005a). Average histamine
levels were recorded at 91 mg/kg after just 9 days at 4°C (Du et al. 2002), a more likely
commercial scenario in New Zealand. Histamine levels in tuna chunks containing relatively high
levels of histamine-producing bacteria were reported to increase from 4.5 to 46.6 mg/kg after
just 48 h in ice (Jeyasekaran et al. 2006). In dophinfish at 26°C, more than12 h of incubation
was required before a histamine concentration of 50 mg/kg was reached while at 35°C this level
4366 July 2010 Research review: histamine poisoning in fish Page 29
was formed within 9 h (Staruszkiewicz et al. 2004). Histamine levels exceeded 500 mg/kg within
an additional 3 h of incubation at 35°C and similar results were found for skipjack and yellowfin
tuna (Staruszkiewicz et al. 2004). Although histamine is formed by the decarboxylation of
histidine in fish, there was poor correlation between decreases of histidine in dophinfish and
increases in histamine (Antoine et al. 2002b). Eight days’ storage at 5°C only resulted in 6
mg/kg histamine in tuna but at 20 and 30°C, histamine formation in mackerel and tuna
exceeded 500 mg/kg within 1 and 2 days respectively (Ohashi 2002). Similarly histamine levels
exceeded 100 mg/kg in Atlantic mackerel held at 25°C for 24 h but not when held at 4°C for 3
days (Merialdi et al. 2001). Histamine levels in Indian anchovies remained below 20 mg/kg
during 15 days’ storage in ice but were around 200 mg/kg after 32 h at 15°C and 8 h at 35°C
(Sureelak et al. 2005). Histamine levels in black skipjack tuna remained below 50 mg/kg during
24 days’ storage in ice (Mazorra-Manzano et al. 2000). Tropical barracuda (Sphyraena
barracuda) did not show major increases in histamine-producing bacteria during 6 h at an
ambient temperature of 32°C although sensory shelf-life was decreased by 6 days
(Jeyasekaran et al. 2004). Auerswald et al. (2006) reported that histamine levels in barracouta
exceeded 500 mg/kg after 4 days at 4°C (implicating psychrotrophic bacteria) and 1 day at
30°C. Shin-hee et al. (2001a) found that significant amounts of histamine were produced in
Pacific mackerel stored for up to 14 days at 1°C but not 0°C and the optimum temperature for
histamine production was 25°C.
Repeated short times at high temperatures can have can have a cumulative impact on
histamine production, somewhat similar to that predicted from continuous storage at high
temperatures for a similar time period. For example, tuna loins stored for 2 h periods at 20°C
each day gave histamine levels of 260 mg/kg after 12 days when stored the rest of the time at
0–2°C and gave levels of 430 mg/kg after 4 days’ storage at 6–7°C with daily 2 h periods at
30°C (Economou et al. 2007).
The rate of histamine production appeared to be higher in summer-caught mackerel compared
to winter-caught fish when stored under refrigerated temperatures (3 rather than 4 days to
exceed 100 mg/kg) (Vusilovic et al. 2008). Similar results were found when fish were stored at
ambient temperatures (2 rather than 3 days to exceed 100 mg/kg for summer- and winter-
caught mackerel), but presumably the ambient temperature was higher in summer (Vusilovic et
al. 2008). In Peru, fish purchased from retail markets later in the day (with longer storage times)
had higher histamine levels than those purchased earlier (Gonzaga et al. 2009).
Among processed products, Mahendradatta et al. (2003) found Lawa teri (fresh anchovy mixed
with citrus juice or vinegar and fried coconut) to give the highest levels of histamine (230 mg/kg)
during 2 weeks’ storage at just 5°C. Feseekh (Egyptian salted-fermented fish) was safe during
40 days’ storage but exceeded tolerance limits (200 mg/kg) by 60 days (Rabie et al. 2009).
Strong correlations have been made between sensory deterioration and the levels of histamines
and other biogenic amines, e.g. in dophinfish (Antoine et al. 2004). Consequently, levels of
biogenic amines have been used as a useful objective quality indicator: for a number of fish
species they increase as sensory quality decreases (e.g. Jeya Shakila et al. 2001; e.g. Antoine
et al. 2004). In bigeye tuna steaks (Thunnus obesus) and whole skipjack tuna (Katsuwonus
pelamis) cadaverine appeared prior to and/or accumulated at a faster rate than histamine so
was proposed as an index of decomposition either alone or in combination with histamine
(Rossi et al. 2002). Staruszkiewicz et al. (2004) also noted that cadaverine levels in dophinfish
and tuna increased before histamine. However, K. oxytoca produced cadaverine over a wide
range of temperatures but only produced histamine at room temperatures (Veciana-Nogues et
Page 30 4366 July 2010 Research review: histamine poisoning in fish
al. 2004) so using cadaverine as a pre-emptive predictor of histamine would likely result in many
false positive predictions. Guizani et al. (2005) reports that yellowfin tuna (Thunnus albacares)
was rejected by sensory panellists before it reached toxic histamine levels. These authors
recorded unacceptable levels of histamine after just 1 day at 20°C or 4 days at 8°C. At 0°C they
recorded declines in histamine levels. Whole ungutted sardines (Sardina pilchardus) were
reported to develop histamine levels above legal limits after 7 days’ storage in ice but the
sardines were rejected by sensory panels by that time (Erkan & Ozden 2008).Tuna fillets stored
for 9 days at 22°C were considered unacceptable from a sensory perspective. However, a
sensory panel had not rejected tuna stored for 3 days when histamine averaged 1000 mg/kg
(Du et al. 2002). Up to 75% of an experienced untrained panel rated the odour of bluefish
(Pomatomus salatrix) that was either inoculated or uninoculated with M. morganii as acceptable
(Lorca et al. 2001). These results confirm our findings that while spoilage usually occurs as
histamine levels increase, sensory evaluation is sometimes but not always sufficient to assure
safety (Fletcher et al. 1995).
4.6 Controls
4.6.1 Rapid refrigeration
The most commonly recommended method for preventing histamine poisoning is to rapidly chill
susceptible fish to slow down or prevent the growth of the bacteria that produce histamine. The
most commonly applied recommendations in this regards are those of the US Sea Grant
Extension Program (Lampila & Tom 2009). Recommendations include:
Generally, fish should be placed in ice or in refrigerated seawater or brine at 4.4°C or less within 12 h of death, or placed in refrigerated seawater or brine at 10°C or less within 9 h of death;
Fish exposed to air or water temperatures above 28.3°C, or large tuna (i.e. above 9 kg) that are eviscerated before on-board chilling, should be placed in ice (including packing the belly cavity of large tuna with ice) or in refrigerated seawater or brine at 4.4°C or less within 6 h of death;
Large tuna (i.e., above 9 kg) that are not eviscerated before on-board chilling should be chilled to an internal temperature of 10°C or less within 6 h of death.
It is quite possible that some of the products causing problems in New Zealand are through the
first recommendation not being met. Based on research with tuna, Lampila & Tom (2009)
indicate that the safe shelf-life can be as little as 5 to 7 days for product stored at 4.4°C and any
exposure time above 4.4°C significantly reduces the expected safe shelf-life. In some instances
New Zealand fish that have caused outbreaks may have been stored longer than this or at
higher temperatures before being smoked. However, work on kahawai suggests that as long as
temperatures do not exceed 4.4°C, this fish can be stored for longer periods without increases
in histamine (Section 3.2).
Tuna left hooked on the line for up to 20 h were suspected to have contributed to an outbreak of
histamine poisoning in Pennsylvania (Maher et al. 2000). It is quite possible that the time
between capture and landing on a boat also contributes to the high number of poisonings from
kahawai in New Zealand. This fish is usually caught by gillnetting from small fishing dories and
the fish may be left in the net for considerable time before landing on the boat and being iced.
Histamine (or at least high levels of histamine-producing bacteria) and perhaps histidine
decarboxylase may be produced during this time. That many of the outbreaks occur in summer
when water temperatures are higher would support this hypothesis. The effect on levels of
4366 July 2010 Research review: histamine poisoning in fish Page 31
histamine and histamine producing bacteria of the time between capture and landing on the
boat should be researched. The effect of fish struggling in the net should also be investigated.
4.6.2 Heading, gutting and skinning
As many of the naturally occurring histamine-producing bacteria are present on the gills, skin
and in the guts of freshly harvested fish, early removal of any of these may delay histamine
production. For example, delayed gutting increased histamine development during the ripening
of European anchovies (Engraulis encrasicholus) (Pons-Sanchez-Cascado et al. 2003).
4.6.3 Heat processing
Histamine is relatively heat-stable and is not eliminated by canning: canned products are
recorded to contain high levels of histamine on occasion (>1000 mg/kg) in some markets (Erkan
et al. 2001; Hyoungill et al. 2005) and have caused outbreaks of food poisoning in New Zealand
(Foo 1975b). Canned mackerel was responsible for a 2001 outbreak of histamine poisoning in
Taiwan and incriminated product contained 1540 mg/kg histamine (Yung-Hsiang et al. 2005b).
The histamine in canned products is presumably formed before canning in that histamine
forming bacteria are not detected in the canned products (Hyoungill et al. 2005). However,
although not eliminated, histamine levels are definitely reduced by canning (Baygar & Gokoglu
2004) so heat processing does mitigate the risk to some degree.
Heat processing below canning requirements can be used to inactivate histamine-producing
bacteria before histamine is formed as described for hot smoked fish in Section 3.3. Emborg &
Dalgaard (2008a) determined the inactivation dynamics of M. morganii and M. psychrotolerans
in Luria Bertani broth with amino acids and lactic acid added to match the levels found in tuna.
Predictably, the psychrotrophic M. psychrotolerans was more heat-sensitive than the mesophilic
M. morganii (Emborg & Dalgaard 2008a) with D values of 5.3 min and 13.1 min and z-values of
6.8 and 7.2°C respectively. These M. morganii results suggest more heat resistance than we
found working with M. morganii associated with hot-smoked kahawai (Osborne & Bremer 2000).
Components of the hot-smoked kahawai might have sensitised the cells to heat inactivation.
4.6.4 Smoked and salted fish
Little work has been done internationally on hot-smoked fish. Zotos et al. (2001) concluded that
histamine levels did not exceed 75 mg/kg immediately after smoking tuna under a number of
different configurations, but they did not appear to test increases in histamine during storage
despite storing vacuum packed product for 3 months at 5°C. Histamine levels in yellowfin tuna
were reported to increase to 12 mg/kg during mild hot-smoking (70°C, 2 h) whilst numbers of
amine-producing bacteria decreased but were not eliminated (Shakila et al. 2003). Predominant
amine-forming bacteria identified were Micrococcus, Alcaligenes and Corynebacterium. While
the temperature within the smoker was monitored, these researchers (Shakila et al. 2003) did
not measure actual product temperatures, and it is likely that product temperatures did not
reach the levels we recommended to inactivate vegetative bacterial hazards or those
determined to inactivate M. morganii (Osborne & Bremer 2000) or H. alvei (Bremer et al. 1998).
However, given the low levels of histamine produced during smoking, Shakila et al. (2003)
suggest that histamine development in smoked yellowfin tuna may be predominantly associated
with delays in the hot blanching performed before smoking or delays in smoking, which is
possibly the case in New Zealand as well.
Page 32 4366 July 2010 Research review: histamine poisoning in fish
Emborg & Dalgaard (2006) found that cold-smoked tuna that caused outbreaks had low
(1.3–2.2%) water phase salt (WPS) compared to other commercially available product
(4.1–12.7%). They found that although M. psychrotolerans grew at a WPS of 4.4%, at 6.9% the
microflora was dominated by benign lactic acid bacteria and neither M. psychrotolerans nor P.
phosphoreum grew. They therefore recommended WPS of >5% to prevent histamine formation.
This is quite high for New Zealand smoked products and goes against dietary recommendations
to reduce salt intake. For hot-smoked products we would generally recommend relying on the
heat process to eliminate histamine-producing bacteria rather than adding high levels of salt to
prevent their growth (Fletcher et al. 1998a). Hazard analysis and critical control point (HACCP)
plans to control storage temperatures and fish quality controls to ensure that fish has not been
stored for too long before smoking are also required to prevent histamine forming before
smoking.
Polish salted herrings prepared in high salt (26%) brines did not produce any histamine when
stored at 4 or 22°C, and those prepared in low salt (16%) brines only produced 35 mg/kg during
3 weeks of storage (Fonberg-Broczek et al. 2003). When salting Spanish mackerel at fish:salt
levels of 1:1, 2:1 and 3:1 by weight, Orawan & Pantip (2000) found that histamine levels
respectively increased to 1155, 1583 and 1251 mg/kg during the first 6 days as salt levels
increased to 15%, but subsequently decreased as salt levels increased to19%. High salt levels
(20 or 23 g/L in the aqueous phase) in anchovy paste stored for 1 year prevented histamine
production (Pirazzoli et al. 2006). As histamine levels did not relate to bacterial numbers, these
researchers suggest that the histamine might have been due to the presence of preformed
histidine decarboxylase in the anchovies.
4.6.5 Modified atmosphere packaging
Some modified atmosphere packaging (MAP) conditions have been reported to reduce the
formation of histamine in susceptible products. A CO2:O2:N2 gas mix of 40:40:20 inhibited
histamine production in bigeye tuna (Thunnus obesus) whereas fish packed in a 60:15:25 mix or
air resulted in product exceeding 100 mg/kg histamine during 33 days’ storage at 2°C (Ruiz-
Capillas & Moral 2005). Aytac et al.(2000) found that MAP in 100% CO2 (preferably combined
with 5% NaCl) inhibited growth and histamine production of M. morganii. MAP (60% CO2:40%
N2) decreased histamine production in Atlantic herring compared to air storage at 2°C or in ice
(Özogul et al. 2002a, 2002b). Similar results were recorded for sardines at 4°C (Özogul et al.
2004). Emborg et al. (2005) found that although vacuum packaging and MAP in an atmosphere
of 60% CO2:40% N2 did not prevent the development of M. psychrotolerans in tuna, MAP
storage in an atmosphere of 40% CO2:60% O2 did. As no histamine was produced in tuna
storage under this gas mix for 28 days at 1°C, they suggested that it be used instead of vacuum
packing for cold storage of fresh tuna. However, they did not report whether storing tuna under
atmospheres with high O2 had any sensory effects. Having identified P. phosphoreum as an
important psychrotrophic histamine producer in garfish stored at 5°C, Dalgaard et al. (2006)
found that MAP did not reduce histamine production by this organism. P. phosphoreum is well
reported as a major spoilage organism of fish packaged under modified atmosphere packaging,
and although the growth of P. phosphoreum was reduced by CO2, histamine production was
higher in an atmosphere containing 60% CO2:15% O2:25% N2 than in air (Lopez-Caballero et al.
2002).
Vacuum packaging was not found to control histamine production in seer fish (Scomberomorus
commersonii) although it did increase shelf-life, presumably reducing the margin of safety
between spoilage and histamine production (Jeya Shakila et al. 2005b). Vacuum packaging was
4366 July 2010 Research review: histamine poisoning in fish Page 33
reported to increase histamine production in herring compared to ice storage (Özogul et al.
2002b) although the reverse was true in sardines at 4°C. The use of an oxygen scavenger to
remove oxygen from packs was also reported to significantly decrease histamine production in
seer fish while also increasing shelf-life (Mohan et al. 2009).
4.6.6 Freezing and chilled storage
Freezing can reduce histamine formation both by preventing the growth of histamine-producing
bacteria and by reducing the activity of pre-formed histidine decarboxylase. Thus, histamine
production in anchovies was greatest at storage temperatures above 20°C but frozen storage
decreased the rate of production (Rossano et al. 2006). Dalgaard et al. (2006) observed that
because P. phosphoreum is resistant to CO2, it cannot be controlled by modified atmosphere
packaging, but because it is very sensitive to freezing it can be controlled by freezing and
thawing of the product. Thawed fish showed marked reductions in histamine formation when
stored at 5°C. Economou et al. (2007) also noted reductions in histamine formation in thawed
tuna compared to fresh tuna. In contrast, Kim et al. (2002a) found that histamine accumulated
rapidly when thawed fish was stored at 25°C. This may relate to pre-formed histidine
decarboxylase or to the survival of heat-resistant histamine-producing bacteria other than
P. phosphoreum. Staruszkiewicz et al. (2004) also demonstrated that histidine decarboxylase
activity could be retained in frozen fish and could cause increases in histamine levels on
thawing. Yung-Hsiang et al. (2005c) found that although histamine production stopped when
fish were frozen, once samples were thawed histamine accumulated rapid exceeding 500 mg/kg
within 36 h at 25°C. Thus, freezing may limit histamine production while product is frozen but
will not necessarily prevent its occurrence in thawed fish.
4.6.7 Gamma irradiation
Irradiation has been shown to inhibit growth and histamine production of M. morganii in
mackerel fillets (Aytac et al. 2000) and to reduce histamine content in bonito in a dose-
dependent fashion (Mbarki et al. 2008). Irradiation of vacuum-packed chub mackerel (Scomber
japonicus) with a low dose of 1.5 kGy doubled shelf-life (from 7 to 14 days) and reduced
histamine production during that time (Mbarki et al. 2009). When blue jack mackerel (Trachurus
picturatus) was stored for 7 days in ice, histamine levels exceeded 100 mg/kg within 7 days
while in fish that had been irradiated with 3 kGy histamine only reached 54 mg/kg after 23 days
(Mendes et al. 2000). Histamine levels approached 100 mg/kg in Atlantic horse mackerel
(Trachurus trachurus) during 23 days’ ice storage, while no histamine was detected in fish that
had been irradiated at 1 kGy during this time (Mendes et al. 2005). Thus, irradiation is an option
to control histamine poisoning but the technology is not approved for use on fish in New
Zealand and there could be consumer resistance.
4.6.8 Additives
When different food additives were tested, glycine was found to be more effective in reducing
the production of histamine and other biogenic amines in Myeolchi-jeot (a Korean salted
fermented fish product) than other additives (sodium chloride, sucrose, glucose, D-sorbitol,
lactic acid, citric acid and sorbic acid) (Jae-Hyung & Han-Joon 2009). In culture, glycine reduced
histamine production by 93% with similar reductions when 5% was included in the Myeolchi-jeot
during the ripening process. Garlic was found to be more effective than other spices (ginger,
green onion, red pepper, clove cinnamon) at reducing the production of histamine and other
biogenic amines in Myeolchi-jeot (Jae-Hyung et al. 2009). However, histamine production was
only reduced by 12% in culture and 9% when garlic was incorporated at 5% during the
Page 34 4366 July 2010 Research review: histamine poisoning in fish
fermentation process. The glycine and garlic acted by inhibiting the growth and histamine
production by histamine-producing bacteria. Other research suggested that including nuka, a
Japanese by-product of rice polishing, may be useful in reducing histamine in fermented fish
products such as fish sauces (Kuda & Miyawaki). The spice Garcinia cambogia inhibited
histidine decarboxylation in homogenised skipjack samples: this was attributed to its effect on
pH (lowered to 3.6) while Tamarindus indica (tamarind) and fruits of Avverhoea bilimbi (bilin) did
not prevent histamine formation (Thadhani et al. 2002).
NaCl (5%) and potassium sorbate (1%) also helped to control the growth and histamine
production of M. morganii in mackerel fillets (Aytac et al. 2000).
Thus, certain additives may assist in preventing histamine poisoning but none are proposed as
reliable methods of control by themselves.
4.6.9 Protective cultures of bacteria
Although histamine is produced by bacteria that produce histidine decarboxylase, some bacteria
produce diamine oxidases capable of degrading histamine. Enes Dapkevicius et al. (2000)
proposed two such lactic acid bacteria as suitable starter cultures for the production of fish
silage. It is possible that such bacteria could also be used in other fermented seafood products
to inactivate or at least prevent the accumulation of histamine in seafood. Staphylococcus
xylosus was proposed as a protective organism that could be used as a starter culture to
prevent histamine production in Korean fermented foods as well as other products (Jae-Hyung
et al. 2008). S. xylosus was able to degrade both histamine and tyramine and also produced a
bacteriocin-like inhibitory substance that had antimicrobial activity against Staphylococcus
licheniformis strains, which are histamine producers themselves. Lactic acid-producing bacteria
that do not actively inhibit histamine-producing bacteria or degrade histamine themselves may
assist in preventing the development of histamine in fermented products by dominating the
microflora (Petaja et al. 2000).
4.7 Applying predictive models
Another way to control histamine production is to monitor temperatures during transport and
storage and use mathematical models to predict when hazardous levels might occur and thus
when to reject product.
Working on jack mackerel, Bermejo et al. (2004) fitted mathematical models for both bacterial
growth and histamine production. From these they concluded that jack mackerel could be stored
for 4.5–5.5 days at 5°C, 1–2 days at 15°C and 17 h to 2 days at 25°C before the quality of
fishmeal produced from the mackerel would be affected,.
Based on work on tuna, Emborg & Dalgaard (2008a) developed mathematical models for
growth, inactivation and histamine production of M. psychrotolerans and M. morganii together in
response to temperature alone and for the growth and histamine production of M.
psychrotolerans in response to combinations of temperature, CO2, AW, and pH (Emborg &
Dalgaard 2008b). Their models were validated by applying them to the results of their own data
and various studies on histamine production in fish found in the literature. Both of these models
have been made freely available in a relatively user-friendly format as part of the Seafood
Safety and Spoilage predictor software (Dalgaard 2009).
4366 July 2010 Research review: histamine poisoning in fish Page 35
5 Conclusions and recommendations
New Zealand seafood continues to cause outbreaks of histamine poisoning and hot-smoked
fish and particularly hot-smoked kahawai are most commonly implicated. Kahawai is a valuable
fish resource and smoked kahawai is a sought after product for consumers. However, fish
companies are shying away from producing it because of fears of potential histamine poisoning.
Although there is a very large body of international literature on histamine poisoning, outbreaks
still occur and some research questions remain: answers to these could help protect consumers
of New Zealand seafood. In previous work (Section 3.4.1) on the microflora, of hot-smoked
products, we assumed that histamine production occurred during or after smoking and that
histamine-forming bacteria had survived the smoking process. We therefore isolated and
identified histamine-producing bacteria from a range of hot-smoked seafoods produced in New
Zealand (Fletcher et al. 1998c), identified them and evaluated their ability to grow and produce
histamine at different temperatures (Section 4.1). Continued failure of hot-smoking facilities to
produce safe products may be because operators of these facilities fail to comply with the
guidelines developed from our work or it may mean that the histamine had already formed
before product arrived at the smokehouse. Recent literature suggests that psychrotrophic
bacteria have a very significant role in histamine poisoning: further work on the role of these
bacteria in the New Zealand environment is warranted. Taking the review commentary
presented above into consideration, our recommendations for monitoring and research into
histamine poisoning in New Zealand include:
1. Agencies investigating food-borne outbreaks of histamine poisoning should carry out
more detailed investigations: if ever possible, the actual remains of the fish causing
outbreaks of histamine poisoning should be tested for levels of histamine and other
biogenic amines; the histamine-producing bacteria involved should be identified and
characterised and results published. If the fish species is in doubt, it would be useful to
identify this by genetic means, such as was done for Taiwanese billfish (Yung-Hsiang et
al. 2007b). Results of such investigations would provide a clearer picture of the factors
contributing to outbreaks of histamine poisoning in New Zealand and help guide the
development of methods to prevent such outbreaks.
2. Some fish species that have been reported to cause histamine poisoning overseas
should be added to the NZFSA list of imported fish species of histamine poisoning
concern so that those handing these species are advised to take extra precautions with
these species as well as those already listed. These include escolar, garfish,
swordfishes and billfishes,
3. In order to quantify the levels of other biogenic amines in outbreak cases and research
studies, HPLC or other methods to effect this need to be reviewed in detail and a
suitable method implemented. Knowledge of other biogenic amines in products causing
outbreaks will allow knowledge gained from New Zealand outbreaks to contribute to
understanding the aetiology of histamine poisoning.
4. The unpublished work summarised in Section 3.4 should be formally published in a
peer-reviewed journal in order to make findings available to the international research
community and to increase understanding of the conditions under which high levels of
histamine can occur. The evidence that histamine is only produced when bacteria enter
the stationary phase should be particularly useful for those developing mathematical
models of histamine production and developing software packages to predict risk of
Page 36 4366 July 2010 Research review: histamine poisoning in fish
histamine poisoning under different conditions. Publication of the research would
necessitate revisiting the identification of the strains using genetic identification
methods.
5. The contribution of psychrotrophic histamine-producing bacteria to the production of
histamine in kahawai and other New Zealand fish should be evaluated. Histamine-
producing bacteria should be isolated from freshly caught and temperature-abused fish
with a focus on psychrotrophic histamine-producing bacteria. Their ability to produce
histamine under different conditions and the conditions required to inactivate these
bacteria should be determined. This information would guide the identification of
hazardous handling practices that present a food safety risk and identify controls to
protect against this.
6. Histamine production in kahawai before smoking should be more fully investigated, in
particular, taking into account the effect of time spent in gill nets before harvest and the
stress to the animals that will occur during this time. This could lead to identifying other
hazardous practices and to future seafood management guidelines for safer harvesting
methodologies and technologies.
7. Methods to evaluate the quality of kahawai (and other hazardous species) at the point
of smoking should be defined so that these can accurately be performed by industry. A
quality index method was used in earlier research (Fletcher et al. 1995), but this has not
been validated. Practical quality thresholds that can be applied by industry are needed
and this research would help industry to reject fish that have been stored for too long or
at too high temperatures rather than smoking them.
8. Factors that increase histamine production without excessively increasing sensory
spoilage should be more closely evaluated. Most studies suggest that by the time
excessive levels of histamine are formed, the product would already be rejected by
normal sensory evaluation. However, the number of food poisoning incidents from
smoked kahawai where high levels of histamine have been found in product show that
this may not be the case for this product. Research should determine why such
incidents happen and what circumstances lead to products containing high levels of
histamine having sensory qualities that are acceptable to consumers. Understanding
this may lead to other measures that might indicate that fish are potentially hazardous.
4366 July 2010 Research review: histamine poisoning in fish Page 37
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