Research of relevance to histamine poisoning in New · PDF fileResearch of relevance to...

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

Disclaimer Unless agreed otherwise, The New Zealand Institute for Plant & Food Research Limited does not give any prediction, warranty or assurance in relation to the accuracy of or fitness for any particular use or application of, any information or scientific or other result contained in this report. Neither Plant & Food Research nor any of its employees shall be liable for any cost (including legal costs), claim, liability, loss, damage, injury or the like, which may be suffered or incurred as a direct or indirect result of the reliance by any person on any information contained in this report. This report has been prepared by The New Zealand Institute for Plant & Food Research Limited (Plant & Food Research), which has its Head Office at 120 Mt Albert Rd, Mt Albert, Auckland. This report has been approved by: Graham C Fletcher Scientist/Researcher, Food Processing and Preservation Date: 30 July 2010 Jocelyn Eason Science Group Leader, Postharvest Fresh Foods Date: 30 July 2010 Requests for further copies should be directed to: Publication Adviser MAF Information Bureau P O Box 2526 WELLINGTON Telephone: 0800 00 83 33 This publication is also available on the MAF website at: www.foodsafety.govt.nz/science/research-projects/reports-projects/ © Crown Copyright, 2011 - Ministry of Agriculture and Forestry

http://www.foodsafety.govt.nz/science/research-projects/reports-projects/

Contents

Executive summary i

1 Introduction 1

2 Histamine poisoning in New Zealand 3

3 New Zealand research 5 3.1 Retail surveys 5

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3.4 Unpublished New Zealand research 8 3.4.1 Identification of histamine-producing bacteria in hot-smoked fish 8 3.4.2 Growth of individual bacterial strains in broth 9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

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.


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

kahawai, summer, 8000 mg/kg), Foo (1975a) (kingfish, 7580 mg/kg), Mitchell (1984) (smoked

kahawai, 2000 mg/kg; kingfish, 6000 mg/kg), Mitchell & O’Brien (1992) (smoked mackerel,

summer, 3000 mg/kg) and Thornton & Calder (1993) (smoked Spanish mackerel, December,

3000 mg/kg). Mitchell (1993) reported a cluster of 19 samples suspected of causing histamine

poisoning between January 1990 and June 1993 with the following implicated products (and

sample numbers): smoked kahawai (6), smoked marlin (3), smoked mackerel (4), 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.


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

2006 February Auckland Fish Supermarket 4C, 2P

2006 November Auckland Smoked kahawai Fisk smoking plant, supermarket 2C 2, 5

2006 February Rotorua Kingfish Restaurant/café 4P

2007 January Northland Fish cakes Takeaway 5C

2007 September Auckland Tuna and marlin Fish processing premise 3P

2008 January Auckland Smoked kahawai Home, open air market 2P

2008 November Auckland Smoked kahawai Home 4C

2009 February Auckland King fish Restaurant/Cafe 3P

*C=confirmed, P = probable


3 New Zealand research

As mentioned above, Plant & Food Research (then Crop & Food Research and DSIR) carried

out work on the issue of histamine poisoning from hot-smoked fish in the late 1980s and 90s

with a focus on identifying the levels, development and inactivation of histamine-producing

bacteria and histamine in smoked fish, particularly kahawai. These published studies are

reviewed here. As we also completed a significant body of research on the growth and

histamine production of individual strains of bacteria that has not yet been formally published

these results are also presented in Section 3.4.

3.1 Retail surveys

3.1.1 Histidine levels in whole New Zealand fish of various species

To identify New Zealand species that might present a health risk to consumers, we determined

the levels of free histidine present in the flesh of species on the local retail market (Fletcher et

al. 1995). Fresh whole fish (47) from 28 species were purchased from Auckland retailers and

levels of histidine and histamine were determined. The species could be divided into three

groups on the basis of their histidine levels. Species with histidine levels above 10,000 mg/kg

(albacore, kingfish and kahawai) had all previously been implicated in histamine poisoning. The

other pelagic species (grey mullet, trevally, sprat, piper, jack mackerel, yellowtail, blue mackerel

and barracouta) had histidine levels between 2000 and 10,000 mg/kg. Of these species, only

mackerels had at that time formally been implicated in histamine poisoning in New Zealand (Foo

1975b; Mitchell & O'Brien 1992; Thornton & Calder 1993). However, we recorded histamine

levels above 100 mg/kg for several other species in the Auckland retail market (Fletcher et al.

1998c and unpublished data). We therefore concluded that these species all have the potential

to cause histamine poisoning. Subsequently, trevally has been implicated in outbreaks (Table

1). The remaining 17 species tested were all demersal species with histidine levels of less than

2000 mg/kg and are not expected to pose any risk from histamine poisoning.

3.1.2 Levels of histamine and histamine-producing bacteria in hot-smoked fish

In the retail survey described above, five of the 47 whole fish examined had histamine levels

above 100 mg/kg (an albacore tuna, a kingfish, a kahawai and two jack mackerels) (Fletcher et

al. 1995). However, as all New Zealand histamine poisoning incidents in the 10 years to 1997

involved hot-smoked fish, our subsequent work focused on this product. We purchased samples

of smoked fish (107) from 9 Auckland retailers over a 9-month period and determined aerobic

plate counts at 20 C (APC), histamine and moisture levels (Fletcher et al. 1998c). Eight

samples, obtained from five different retailers, had histamine levels above 50 mg/kg and levels

in two samples (346.4 and 681.8 mg/kg) exceeded 200 mg/kg. We stored 33 of the smoked fish

samples at 20 C for 2 days and 8 of these developed histamine levels above 50 mg/kg with 4

exceeding 200 mg/kg (maximum 1659.4 mg/kg). The four stored samples exceeding 200 mg/kg

all came from two outlets. Bacterial strains (3525) were isolated by selective plating on to

Niven’s agar or by picking colonies from trypticase soy agar (TSA) incubated at 5, 20 or 35 C.

Strains were tested for their ability to produce histamine in a histidine-saline solution containing

just histidine (2 g/L) and NaCl (5 g/L). Although isolated at a range of different temperatures

from refrigerated product, 97.6% of the 3525 tested cultures grew at 20 C so we conclude that

an isolation temperature of 20°C is suitable for most psychrotrophic as well as mesophilic

organisms. This is in line with other work that we have done on psychrotrophic bacteria from


seafood (Weirda et al. 2006). Other studies suggest 15°C or less as suitable isolation

temperatures for psychrotrophic bacteria, e.g. (Dalgaard et al. 1998), but this typically

necessitates separately incubating samples under higher temperatures to isolate mesophilic

bacteria, which would increase both time and cost of isolation.

After re-inoculating into the histidine-saline solution, only 168 of the tested strains produced

histamine from histidine when log phase cultures were inoculated into the histidine-saline

solution and held for 8 days at 20 C (Fletcher et al. 1998). This low proportion of the tested

strains highlights the fact that few of the bacteria present on smoked fish are capable of

producing histamine. That many organisms from the selective Niven’s agar did not produce

histamine in the broth pointed to the inadequacy of this agar. Many strains that were

presumptive histamine producers in Niven’s agar turned out to be false positives.

3.2 Bacterial growth and histamine production in whole kahawai

We also carried out two trials in which un-inoculated kahawai were stored under 17 temperature

regimes at temperatures between 0 and 35 C (Fletcher et al. 1995). In 10 regimes the fish were

transferred from storage at various elevated temperatures to storage at 5 C in order to mimic

likely commercial practice. Levels of histamine, APCs and sensory quality were monitored.

Elevated histamine levels were first recorded in fish stored for 0.9, 0.9, 1, 2, 2.7, and 8 days at

35, 30, 25, 20, 15 and 10 C respectively (Figure 1b). Storage at 5 C after storage at higher

temperatures did not result in elevated levels. Of the 59 samples with elevated histamine levels,

examination of the raw fish suggested that 9 had acceptable sensory characteristics. However,

all had aerobic plate counts exceeding 106 colony forming units (cfu)/g (Figure 1a).

3.3 Thermal death

Histamine is heat stable and thus, if formed before processing, is not destroyed by hot-smoking

but histamine production subsequent to smoking could be prevented by the thermal elimination

of histamine-producing bacteria during hot-smoking. We therefore determined the thermal death

characteristics of two histamine-producing bacterial species. Under simple linear models, the

thermal death characteristics of bacteria can be fully described by calculating two standard

values: The D value refers to decimal reduction time - the time required at a particular

temperature to cause a 10-fold inactivation (90% reduction) of the organism being studied. The

z value is the change in temperature required to achieve a 10 fold reduction in D value for the

organism. Within the experimental boundaries, once D and z values are known, it is possible to

calculate what level of bacteria will be inactivated at any particular combination of time and

temperature.

3.3.1 Hafnia alvei

H. alvei strains have been implicated in incidents of histamine poisoning and H. alvei was the

histamine-producing bacteria isolated from our sample with the highest histamine level (1659.4

mg/kg). Thermal death trials on our experimental strain of this organism were carried out in a

model suspension (0.1% peptone). Samples containing high levels of H. alvei were subjected to

different temperatures for different times and numbers of surviving bacteria used to calculate

observed D values at the different temperatures. From the linear regression line fitted to the

observed D values plotted against temperature (Figure 5), calculated D values for 54, 55, 56, 57

and 58 C were estimated to be 0.63, 0.36, 0.20, 0.11 and 0.06 min, respectively and a z value


of 4.14 C was calculated. Thermal death trials were also carried out for H. alvei that had been

associated with hot-smoked kahawai. Here the calculated D values for 54, 55, 56, and 57oC

were estimated to be 1.42, 0.74, 0.38, 0.20 min respectively, giving a z value of 3.57oC.

Although the kahawai protected the bacteria from heat compared to when broth was heated, we

still concluded that hot-smoking could be used to eliminate H. alvei from seafood products

(Bremer et al. 1998).

3.3.2 Morganella morganii

As growth trials (Section 3.3.2) indicated that M. morganii was the most important bacterium for

histamine production in hot-smoked kahawai, we investigated the thermal death characteristics

of the nine strains (including a culture collection strain) that we had of this organism (Osborne &

Bremer 2000). A mixed inoculum was added to kahawai mince and a variation of the Bigelow or

z-value model was used to generate a thermal death time graph. The production of histamine, in

a heat-treated and subsequently temperature-abused sample, was scored as a positive value

(growth) and the absence of histamine was scored as a negative value (no growth).

Temperatures tested were 58, 59, 60, 61 and 62 C. From the straight line fitted to the data

(Figure 6), calculated times for eliminating histamine-forming bacteria were estimated to be

15.27, 4.79, 1.46 and 0.04 min respectively, giving a z value of 3.85 C. This approach to

thermal death determination based on the presence/absence of a bacterial metabolite was an

efficient way to determine the thermal regime required to eliminate histamine-producing bacteria

from kahawai. Again, we concluded that M. morganii could be eliminated by the hot-smoking

process.


b. Growth and histamine production in

whole kahwai stored at various temperatures

Time from capture (days)

0 2 4 6 8

Mea

n a

ero

bic

pla

te c

ou

nt

(20°C

)

(lo

g1

0cfu

/g)

3

4

5

6

7

8

9

D-V

alu

e

(min

ute

s)

Temperature (°C)

Time from capture (days)

0 2 4 6 8

Mea

n h

ista

min

e

(mg

/kg

)

0

1000

2000

3000

10°C

15°C

20°C

25°C

30°C

35°C

a. Histamine production vs bacterial counts

in kahawai flesh

Count of individual samples (log10cfu/mL or g)

2 3 4 5 6 7 8 9 10 11

His

tam

ine

lev

el

of

ind

ivid

ual

sa

mp

les

(mg

/L o

r m

g/k

g)

0

1000

2000

3000

4000

5000

6000

c. Thermal death times of Hafnia alvei

at various temperatures

53 54 55 56 57 58 59

0.1

1

10

d. Core temperatures/times required to

ensure a final product that will not produce

histamine during subsequent temperature abuse

Temperature (°C)

57 58 59 60 61 62 63

Tim

e

(min

ute

s)

0.1

1

10

100Histamine production by M. morganiiNo histamine production by M. morganii

Inactivation in kahawai minceInactivation in broth

Figure1. Results from published studies on growth, histamine production and inactivation of total bacterial flora in kahawai flesh.

3.4 Unpublished New Zealand research

As well as the published results presented above, we (Graham Fletcher, Scott Speed, Graeme

Summers and Tricia Lee) also carried out a considerable amount of work on the identification

and growth of histamine-producing bacteria isolated from smoked fish. We made several oral

presentations (Fletcher et al. 1998b; Fletcher et al. 1999; Fletcher & Bremer 1999), but this work

had not been published at the conclusion of the project. Key findings are summarised below.

3.4.1 Identification of histamine-producing bacteria in hot-smoked fish

The 168 strains of histamine-producing bacteria isolated from hot-smoked fish (Fletcher et al.

1998c) were identified using API 32, API 20NE and API 20E strips (BioMérieux, Lyon, France)

and/or by using fatty acid methyl ester analysis (Microbial Identification Inc (MIDI), Newark,

Delaware USA). One hundred and thirty-five strains were successfully identified, at least to the

genus level, and these consisted of: Pseudomonas (81), Serratia (10), Morganella morganii (9),

Hafnia alvei (9), Chryseomonas (8), Staphylococcus (4), Moellerella (4), Acinetobacter (2),

Enterobacter (2), Alcaligenes (1), Bacillus (1), Brochothrix (1), Flavobacterium (1), Cellulomonas

(1) and Moraxella (1). At the time this seemingly simple task required considerable effort

because many of the test methods gave unacceptable or unknown profiles. Further phenotypic

testing might have provided better clarification, but these were not completed due to constraints


of budget and time and it is likely that many of these organisms would still have been difficult to

speciate with the phenotypic methods available at the time. Modern genotypic identification

methods are more likely to yield more definitive results, and the cost of doing these are now

comparable or cheaper than using phenotypic testing.

3.4.2 Growth of individual bacterial strains in broth

Experiments were conducted to assess the growth and histamine production ability of different

strains of histamine-producing bacteria isolated from hot-smoked fish. Thirty-nine of the strains

collected from different samples with elevated levels of histamine (>50 mg/kg) were selected for

growth studies: (Morganella morganii (8), Hafnia alvei (2), Pseudomonas (16), Serratia (7),

Acinetobacter (2), Alcaligenes (1), Moraxella (1), Moellerella (1), and Cellulomonas (1)).

Because it has been most implicated in international outbreaks of histamine poisoning, we

thought it valuable to see whether the New Zealand isolated stains of M. morganii showed major

differences to international strains: we therefore added a culture collection strain of this

organism, giving a total of 40 strains to be used in growth experiments. We prepared kahawai

broth from fresh kahawai muscle after the method of Omura et al. (1978) and determined the

growth characteristics of each organism and the production of histamine in broth. Experiments

on each culture were conducted at 0, 5, 10, 15 and 20 C with 5 sampling times spread over

periods of 27, 12, 7, 4 and 3 days at the respective temperatures (see sampling points in Figure

2b). On each occasion bacterial counts were determined on plate count agar (Difco) with 1%

added NaCl using the drop plate method and histamine levels were determined using the AOAC

method (Association of Official Analytical Chemists 1990).

Initial bacterial counts varied with the different experiments, ranging from 2.354 to 5.288 log10

cfu/g. Predictably, some strains showed characteristics of psychrotrophic genera

(Pseudomonas, Alcaligenes, Moellerella, Moraxella and Serratia) growing to high levels

(108–10

10 cfu/g) at all tested temperatures while others (Cellulomonas and M. morganii) only

grew at mesophilic temperatures (i.e.10°C or higher) and under the conditions of these

experiments only reached high levels at 15 and 20°C. The two Acinetobacter strains grew at

temperatures of 5°C and above but not 0°C. One of the H. alvei strains also grew at 5°C and

above but not 0°C, while the other grew to high levels at all temperatures. Initial histamine levels

in the kahawai broth averaged 1.87 mg/L. All 9 strains of M. morganii produced elevated

histamine levels (>50 mg/L), but only one strain of each of four other species did: H. alvei (the

strain that didn’t grow at 0°C), Alcaligenes, Pseudomonas and Serratia. Thus, a total of 27 of 40

strains that produced histamine in the histidine-salt solution did not do so in the more complex

kahawai broth.

As M. morganella was the most prolific histamine-producing species found in smoked fish and

the one most able to produce histamine over a range of conditions, we focused our analysis of

results on this species. Curves were fitted to the growth results for each of the nine strains. As

we only had one replicate growth curve for each of the strains and only a few points during the

logarithmic growth phase, the accuracy of the growth rates is relatively low. However, analyses

showed that none of the strains was significantly different to the others (e.g. see Figure 2a) so

the bacterial growth rates at the different temperatures were averaged across the strains to give

mean growth rates for the species as shown in Figure 2b, upper plot. Production of histamine by

M. morganii was related to its growth (Figure 2b, lower plot), never producing elevated

histamine levels at 0 or 5 C and only after more than 5 days at 10 C, 1 day at 15 C and 12 h at

20 C. When it occurred, histamine production invariably began as the bacteria entered the

stationary growth phase (> 108 cfu/mL) (Figure 2b). This result is in general agreement with


those found in the whole fish and the temperature response and storage times required before

histamine production occurred were also similar (compare Figures 1b and 2b). However, the

actual bacterial counts at which histamine production was initiated were higher and levels of

histamine produced were lower in the broths than in the kahawai (compare Figures 1a and 2c).

A possible explanation for the higher counts might be that nutrients are more readily available to

the bacteria in the broth than in the intact kahawai flesh so they reached higher levels before

entering into the stationary phase, which may be initiated by nutrient limitation. Histamine

production was still only initiated when bacterial growth entered the stationary phase, but the

stationary phase in the broth occurred at a higher concentration of bacteria than in the fish. This

supports the hypothesis that, although bacteria may have the capability to produce histamine to

gain some metabolic benefit, they tend to only do so when other nutrients are limited. The fact

that 25 of 40 bacterial strains produced histamine in a very low nutrient environment (histidine

plus NaCl) but not in a nutrient-rich kahawai broth supports this hypothesis. The approximately

6-fold higher levels of histamine per kilogram reached in whole fish than in the broths per litre

may simply reflect reduced levels of histidine in the broths, providing less substrate for histidine

decarboxylase enzyme activity that produces histamine. The process of producing broth from

kahawai flesh effectively involved a 1:4 dilution; measured histidine levels in the broth

suggested that reductions in histidine levels were even greater than 1:4.

c. Histamine production vs bacterial counts

in kahawai broth

Bacterial count of individual samples (log10cfu/mL)

2 3 4 5 6 7 8 9 10 11

His

tam

ine

lev

el

of

ind

ivid

ual

sa

mp

les

(mg

/L o

r m

g/k

g)

0

1000

2000

3000

4000

5000

6000

a. Growth of Morganella morganii strains (9) in kahawai broth at 20°C

Incubation (days)

0 1 2 3

Co

un

t (l

og

10cfu

/mL

)

3

4

5

6

7

8

9

10

Smoked fish strains

Type strain

b. Average growth and histamine production of Morganella morganii in kahawai broth

Mean

co

un

t o

f

M.

mo

rgan

ii

(lo

g1

0cfu

/mL

)

3

4

5

6

7

8

9

Mea

n h

ista

min

e(m

g/ m

L)

Incubation (days)

0 5 10 15 20 25 30

0

200

400

600

8000°C

5°C

10°C

15°C

20°C

d. Belehrádek plot of Morganella morganii

growth rates in kahawai broth

Temperature (°C)

0 5 10 15 20 25 30

Sq

uare

ro

ot

of

gro

wth

rate

( [l

og

10cfu

/mL

/da

y]0

.5)

0

1

2

3

Tmin = 4.4°C

985. 0

59. 0 135. 0

2 R

e Temperatur GrowthRate

Figure 2. Results from unpublished studies on growth and histamine production in kahawai broth by Morganella morganii.

985.0

59.0135.0

2R

eTemperaturGrowthRate


We then determined the logarithmic growth rates of M. morganii at the different temperatures

and square roots of growth rates were plotted against temperature (Belehrádek plots) for each

strain. The strains did not differ significantly from each other (Figure 2a) so mean growth rates

at the different temperatures were plotted for the species (Figure 2d) and these showed a linear

relationship with temperature. From this the maximum growth rate at any particular temperature

can be calculated, and in a dynamic real-time situation, the time spent at each temperature can

be used to cumulatively calculate the level of M. morganii that would be present in the broth. As

the growth in broth was faster than in fish, this should provide an overestimation (fail-safe

prediction) for predicting histamine producing bacteria in fish. If our hypothesis that histamine

production begins when bacteria enter the stationary phase is correct, then to predict histamine

production in fish, one would need to know the maximum bacterial count present in fish before

the bacteria go into stationary phase. The Belehrádek plot also gives a theoretical minimal

growth temperature (Tmin the temperature when the growth rate = 0). In the case of M.

morganella, using regression analysis the Tmin was 4.4 C. In practice, bacteria can seldom be

demonstrated to grow at temperatures very close to Tmin, and Belehrádek plots tend to

overestimate growth near Tmin (perhaps due to the stress the organism is under at these

temperatures). Thus, we conclude that M. morganella will not grow below 4.4°C and that

effective refrigerated storage will prevent the growth of this organism.

Similar growth rate and Belehrádek plots were prepared for the other four species of bacteria

that produced histamine at levels above 50 mg/kg (Figures 3–6). These only produced

histamine at 20°C (or 15°C for H. alvei) even though they grew to high levels and usually

reached stationary phase at the other temperatures (Figures 3–6). As none of these species

produced histamine at temperatures below 10°C, we concluded that effective refrigerated

storage will prevent the growth of these organisms. If confirmed in practice this mean that

effective refrigeration (4°C of colder) will prevent histamine production in hot smoked fish.


b. Histamine

Incubation (days)

0 5 10 15 20 25 30

His

tam

ine (

mg

/L)

0

200

4000°C

5°C

10°C

15°C

20°C

Co

un

t (

log

10cfu

/mL

)

3

4

5

6

7

8

9

a. Growth

c. Belehrádek plot of growth rates

Temperature (°C)

-10 -5 0 5 10 15 20 25

Sq

ua

re r

oo

t o

f g

row

th r

ate

( [l

og

10c

fu/m

L/d

ay]0

.5)

0

1

2

3

Tmin = -5.0°C

990.0

8317.04195.0

2R


Figure 3. Growth and histamine production of a Serratia sp. in kahawai broth.


b. Histamine

Incubation (days)

0 5 10 15 20 25 30

His

tam

ine (

mg

/L)

0

200

4000°C

5°C

10°C

15°C

20°C


Temperature (°C)

-10 -5 0 5 10 15 20 25

Sq

uare

ro

ot

of

gro

wth

rate

( [l

og

10cfu

/mL

/da

y]0

.5)

0

1

2

3

Tmin = -10.3°C

997.0

6082.005973.0

2R


Co

un

t (

log

10cfu

/mL

)

4

5

6

7

8

9

10

a. Growth

Figure 4. Growth and histamine production of an Alcaligenes sp. in kahawai broth

997.0

6082.005973.0

2R



b. Histamine

Incubation (days)

0 5 10 15 20 25 30

His

tam

ine (

mg

/L)

0

200

4000°C

5°C

10°C

15°C

20°C


Temperature (°C)

-10 -5 0 5 10 15 20 25

Sq

ua

re r

oo

t o

f g

row

th r

ate

( [l

og

10c

fu/m

L/d

ay]0

.5)

0

1

2

3

Tmin = 0.8°C

991.0

1070.01305.0

2R


Co

un

t (

log

10cfu

/mL

)

4

5

6

7

8

9

10

a. Growth

Figure 5. Growth and histamine production of a strain of H. alvei in kahawai broth

991.0

1070.01305.0

2R




Temperature (°C)

-10 -5 0 5 10 15 20 25

Sq

uare

ro

ot

of

gro

wth

rate

( [l

og

10cfu

/mL

/da

y]0

.5)

0

1

2

3

b. Histamine

Incubation (days)

0 5 10 15 20 25 30

His

tam

ine (

mg

/L)

0

200

4000°C

5°C

10°C

15°C

20°C

Tmin = -7.3°C

Co

un

t (

log

10cfu

/mL

)

4

5

6

7

8

9

10

a. Growth

940.0

0749.05458.0

2R


Figure 6. Growth and histamine production of a Pseudomonas sp. in kahawai broth

Take as an example, Serratia where the Tmin was -5.04°C (Figure 4c): this histamine-producing

organism is well adapted to grow at refrigerated temperatures. However, we found that only one

of the seven strains of Serratia actually produced any histamine in the kahawai broths and then

only when it had reached the stationary phase at 20°C. Thus, although the organism grew well

at refrigeration temperatures, it did not appear to produce any histamine at those temperatures.

Thus, if Serratia produced hazardous levels of histamine in refrigerated fish, these would need

to be stored at refrigerated temperatures long enough for the bacterial colonies to reach the

stationery phase but still no histamine would be produced. They would still have to be held at

ambient temperatures for the bacteria to produce the histamine.

940.0

0749.05458.0

2R



Although carried out more than 10 years ago, no subsequent piece of research has studied the

growth and histamine production of such a wide range of bacteria in such depth. The study brief

did not require publication so a number of the conclusions of the work are not readily available

to the research community. It would, therefore, be beneficial to publish it in an international

peer-reviewed journal. To achieve this it would be necessary to repeat the identification of at

least the 40 organisms used in the study (if not the whole pool of 168 organisms from which

they were taken) using modern genotypic methods.

This unpublished research was carried out with funding by the New Zealand Foundation for

Research Science and Technology. Statistical analyses of the results were carried out by John

Koolard.

3.5 Conclusions and industry recommendations

From our studies we concluded that, under normal circumstances, prevention of histamine

poisoning from hot-smoked fish could be readily achieved by adequate refrigeration (4 C)

before smoking and by ensuring that time-temperature combinations during smoking were

sufficient to eliminate histamine-producing bacteria. We published a set of guidelines for the

safe preparation of hot-smoked fish (Fletcher et al. 1998a) recommending specific refrigeration

regimes for the storage of fish that may be susceptible to histamine poisoning and defining

thermal processing regimes required for the hot-smoke process. Because New Zealand has

also had incidents of listeriosis from hot-smoked seafood, and Listeria monocytogenes is more

thermally resistant than histamine-producing bacteria (Bremer & Osborne 1995), the

recommended thermal regimes were based on L. monocytogenes. As this was one of the first

publications recommending time temperature regimes for the thermal inactivation of vegetative

pathogens in seafood we took a very conservative approach, similar to that used in the canning

industry to control Clostridium botulinum. Thus, we recommended temperature regimes to

achieve an inactivation of 1012

cells of L. monocytogenes which would require a time equivalent

to 12 times the D value (a 12 D reduction). However, in subsequent risk-based

recommendations, if C. botulinum was not the target organism, 6 or 7 D reductions of Listeria

were recommended (Price & Tom 2002a, 2002b). Our guidelines were distributed to all New

Zealand registered producers of hot-smoked fish and relevant regulatory bodies.

As identified in Table 1, the publication and promulgation of these guidelines has not prevented

outbreaks of histamine poisoning from New Zealand hot smoked fish. This may be due to

producers of smoked fish not complying with the guidelines or it may be due to gaps in the

knowledge on which the guidelines were based. One particular such knowledge gap arises

because the research on histamine producers was only carried out on isolates obtained from

hot smoked fish. These organisms had all survived the hot smoking process or were the result

of subsequent contamination. They do not represent the histamine producing bacterial

population that may be present on fish before smoking and the possibility remains that a

different bacterial flora might be responsible for producing high levels of histamine before

smoking. Although these organisms may have been inactivated during the smoking process the

histamine produced before smoking may be that associated with histamine poisoning outbreaks

from smoked fish.


4 Literature update 2000–10

4.1 Other reviews

There have been over 200 publications related to the problem of histamine in fish published in

the scientific literature between 2000 and 2010, including at least five reviews (Lehane & Olley

2000; Mavromatis & Quantick 2002; Shin-Hee et al. 2004; Dalgaard et al. 2008; Al-Bulushi et al.

2009) plus brief summaries in English (Lehane 2000), Spanish (Gonzalez-Dominguez &

Cardona-Galvez 2005) and Serbo-Croat (Cvrtila & Kozacinski 2003). The review by Lehane &

Olley (2000) (for which I served as one of the journal referees) was a reasonably extensive

review of literature (37 pp, 233 references) from a risk perspective covering literature up to

2009. Of particular value was their summary of knowledge on one of the more vexing issues of

histamine fish poisoning – why fish that cause histamine poisoning invariably contain high levels

of histamine but when histamine is fed to people at similar levels in volunteer studies histamine

poisoning does not result. The reviewers hypothesised that cis-urocanic acid, a different break

down product of histidine and a recognised mast cell degranulator might play a role in

augmenting the exogenous histamine. Mavromatis & Quantick (2002) also only reviewed

literature up to 2000 apart from mentioning some surveillance data from post-2000. Reviewing

the mechanism of histamine poisoning they state, ―There is strong evidence that the primary

scombrotoxin is a mast cell degranulator that causes the release of indigenous histamine and

other biologically active substances, which in turn are responsible for the gastrointestinal

symptoms. Therefore, the toxic role of dietary histamine as posed by indigenous histamine is

slight.‖ The review by Shin-Hee et al. (2004) also only covered literature up to 2000 (i.e. similar

to the review by Lehane & Olley) with the exception of some regulatory information, surveillance

data, and some of their own work up to 2003. They conclude that histamine is mostly formed by

a few prolific enteric bacteria such as M. morganella and these are best controlled with proper

chilling and freezing of fish starting at the point of harvesting. Of the two more recent reviews,

that of Al-Bulushi et al. (2009) was quite general, covering a number of biogenic amines and

particularly the possibility of producing nitrosamines from them. Their review was based on the

view that other amines (putrescine and cadaverine) were required to potentiate histamine

poisoning. They concluded that levels of cadaverine and putrescine need to be considered in

any histamine toxicity assessment and that nitrosamine levels should also be closely monitored.

The review by Dalgaard et al. (2008) was more detailed and reasonably comprehensive

although it was somewhat focused on the work carried out in the European BIOCOM project,

which ran from 2004 to 2007. The review by Dalgaard et al. is well worth reading in conjunction

with the current review. Their recommendations include:

1. More investigations of outbreaks of histamine poisoning incidents that examine the

microbiology of the organisms involved, particularly with regard to their

psychrotolerance. Although hundreds of outbreaks are reported each year they could

only find 15 incidents that formally reported on the microbiology involved. Five of these

were their own from which they drew quite different conclusions to those of other

studies.

2. If ever possible investigations are needed to examine the actual remains of meals that

caused the outbreaks. They noted that there are considerable discrepancies in the

literature as to the amounts of histamine required to cause histamine poisoning, but

also noted that while fish from the same batch may be examined, actual meal remains

were seldom examined. However, they note that the levels of histamine vary quite


dramatically from different positions within a fish let alone between fish. They

recommended that outbreak studies should also evaluate the correlation between

histamine and other biogenic amines in agreement with the recommendation of

Al-Bulushi et al. (2009). BIOCOM results suggested that hazard is directly proportional

to histamine levels while others have suggested that other amines are required as

potentiators.

3. Development of mathematical models for growth and histamine production by important

bacterial species other than the model for M. psychrotolerans that was developed under

BIOCOM. They have a model for M. morganella but this only accounted for

temperature, not atmosphere, salt and pH, as included in their model for

M. psychrotolerans. Section 4.3 of the current review shows that there are many other

important histamine-producing bacteria whose growth and histamine production should

be mathematically modelled.

4. More studies on the potential of modified atmosphere packaging (MAP) to control

histamine poisoning. The BIOCOM project suggested combinations of high CO2 and

high O2 might be effective in achieving this.

5. Obtaining more quantitative data on the occurrence of strong histamine-producing

bacteria in marine and seafood processing environments in order to determine how

these organisms come to contaminate fish or whether they are naturally present.

6. More studies on the oral toxicity of histamine, with or without other biogenic amines, to

elucidate the mechanism of action of the intoxication.

4.2 Methods

4.2.1 Extracting biogenic amines from seafood

Standard methods (e.g. AOAC Official Methods 996.07 and 977.13) for extraction of biogenic

amines are based on methanol extraction, but this has sometimes resulted in low recoveries

from fresh fish. Addition of 25% 0.4N HCl to the 75% methanol-water extraction solvent resulted

in histamine recoveries increasing from 54 to 89% in fresh and frozen fish (Richard et al. 2008).

Such acidification did not improve the recovery rate in canned tuna, suggesting that protein

denaturation might also eliminate matrix interference. Supapun & Wararat (2001) used solid

phase extraction to extract histamine from fish sauces. When combined with a high-

performance liquid chromatography-fluorescence (HPLC) detection method (see next section),

recoveries from spiked samples ranged from 90 to 96%.

4.2.2 Measuring histamine and other biogenic amines

Fluorescence detection of histamine has long been the main analytical technique and currently

the most commonly reported method for analysis of histamine is by HPLC detection. For

example, the New Zealand Crown Research Institute, ESR uses an HPLC method based on

that of van Boekel & Arentsen-Stasse (1987). This allows simultaneous detection of histamine

and histidine, which is useful. However, as currently implemented (ESR Auckland Food Group

1996), the ESR method does not allow quantification of other biogenic amines, a procedure that

some researchers consider essential to determine whether products cause histamine poisoning

(Al-Bulushi et al. 2009). There are a number of methods available to simultaneously quantify a

range of biogenic amines in seafood, and a critical review of all of these with a view to


implementing a suitable method is warranted. The EC (Commission of the European

Communities 2005) specifies the method of Malle et al. (Malle et al. 1996) with the standard

additions method of Duflos et al. (Duflos et al. 1999). Reports on detection and quantification in

the last 10 years are reported briefly below.

Various refinements of HPLC technology have been published in the last 10 years, including

development of an automated on-line pre-column derivatisation procedure (Jin-Feng et al. 2008)

and the addition of nucleophilic agents and surfactant micelles to the system (Larionova et al.

2008). Özogul et al (2002a) used benzoyl chloride in acetonitrile as a derivatisation system and

optimised times and conditions with a gradient elution system until it took only 7 min to

determine 9 biogenic amines and trimethylamine (TMA). Niu et al. (2008) developed an HPLC

method with pre-column derivatisation using a newly synthesised fluorogenic reagent

3-(4-chlorobenzoyl)-quinoline-2-carboxaldehyde with recoveries of 95–107%. Qing-Xi et al

(2007) used reverse-phase HPLC with automatic o-phthalaldehyde post-column derivatisation

and fluorescence detection.

Post-column derivatisation capillary electrochromatography with o-phthalaldehyde/N-

acetylcysteine has also been developed to determine biogenic amines (Oguri et al. 2008).

A good correlation (R2 = 0.99) was found between capillary electrophoresis with UV detection

and gas chromatography methods for detecting histamine in dophinfish (Wen-Xian et al. 2001).

A capillary electrophoresis method gave 102% recovery in canned tuna (Paturzo & Bizzozero

2000). A comparison of capillary electrophoresis, the AOAC fluorometric method and GC,

showed a very good correlation (R2 >0.99) for histamine quantification in tuna samples (Du et al.

2002).

Micellular liquid chromatography was reported to give better detection limits than conventional

techniques (Paleologos et al. 2003). An alternative method was developed using micellular

electrokinetic chromatography along with laser induced fluorescence detection using the amino-

reactive chameleon stain Py-1 (Steiner et al. 2009). Derivatisation took 30 min, but was visible

to the naked eye because of a colour change from blue to red.

Simple thin layer chromatography methods using ninhiydrin to visualise the biogenic amines are

suitable for identification and semi-quantification of histamine, cadaverine, putrescine,

tryptamine and tyramine (Valls et al. 2002). Simple colorimetric methods have been developed

(Patange et al. 2005; Kuda et al. 2007) and a colorimetric method was modified to detect

histamine in fish meal (Kose & Hall 2000).

For laboratories that have the technology, gas chromatography/mass spectrometry (GC-MS)

using ethylchloroformate derivative is an option for quantifying histamine and other biogenic

amines (Marks & Anderson 2006). Another gas chromatography (GC) method was developed to

simultaneously detect histamine and cadaverine, but recovery was only 67% for histamine,

compared with 90% for the AOAC fluorometric method (Antoine et al. 2002a). In contrast, a

biosensor based on immobilised diamine oxidase gave comparable results to a HPLC method

(R2 = 0.9612) when used on spiked prawns with a detection limit of 0.65 mg/kg (Ching Mai et al.

2007). The GC method of Bao-Shyung et al.(2003) was also effective, recovering 99–111% of

histamine spiked into shrimp or tuna meat.

There have been a number of rapid methods developed for the successful detection of

histamine based on ELISA and immunochromatography techniques (Berges 2008), biosensor

enzymatic techniques using histamine oxidase for histamine (Frebort et al. 2000; Hibi & Senda


2000) or amine oxidase for total biogenic amines (Muresan et al. 2008). ELISA results were in

good agreement with HPLC for histamine levels below 50 mg/kg but large differences occurred

above this (Vosikis et al. 2008). Japanese researchers have used an oxygen-sensor method

that allows detection of both histamine and K-value (a measure of quality) with the advantage of

being able to report times when histamine levels exceed histamine defect action levels (500

mg/kg) before spoilage occurred (Ohashi 2002). Some of the rapid methods have been

commercialised and Rogers & Staruszkiewicz (2000) compared six of these. All six kits tested

were found to be acceptable for use as screening tests for histamine and were able to

distinguish between products that contained <50 mg/kg and those that contained >50 mg/kg

histamine. A recently developed presence/absence rapid method able to detect 15 mg/kg

histamine in fish and seafood involved adsorption on to a paper disc, electrophoresis for 10 min,

drying and colour development using Pauly's reagent (Sato et al. 2006).

4.2.3 Bacterial methods

Methods for detection of histamine-producing bacteria remain cumbersome with Niven’s agar

being the main selective agar available. However, more than 80% of presumptive positive

cultures on Niven’s agar prove to be negative for histamine production (i.e. false positives)

(Shin-Hee et al. 2001b; Allen et al. 2005). Shin-Hee et al. (2001b) tried several media designed

for other purposes and concluded that the best isolation of prolific histamine producers was

obtained when using Pseudomonas isolation agar for Pseudomonads and eosin methylene blue

(EMB) agar for enteric bacteria. Histamine production had to be confirmed on histidine

decarboxylase differential media (Shin-Hee et al. 2001b). Literature up to 2002 on the detection

of histamine-producing bacteria was reviewed by Shin-Hee et al. (2003a) who recommended

moving to molecular PCR methods.

HPLC was found to be better than Niven’s agar to determine histamine-producing activity in

bacteria, but this required isolating strains and testing them individually (Merialdi et al. 2001).

Some isolated Pseudomonas and Acinetobacter spp. were not identified as histamine producers

by histidine agar, but were shown by HPLC to produce considerable amounts of histamine in a

broth medium (Silva et al. 2002).

Kim et al. (2003) and Shin-Hee et al. (2003b) successfully developed PCR methods to detect

one of the main histamine-producing bacteria, M. Morganii, in albacore tuna, mackerel and

sardines. The method could detect 106–10

8 cfu/g (levels reported to be required for histamine

production) but with 9 h enrichment at 37°C, levels as low as 9 cfu/g could also be detected

(Shin-Hee et al. 2003b). These are promising results but methods would need to be developed

to detect histamine producers other than M. morganii. Takahashi et al. (2003) and Torres Alves

et al. (2002) each developed PCR methods that amplified histidine decarboxylase genes. All 37

tested strains of histamine-producing Gram negative bacteria produced a PCR product, except

Citrobacter braakii, while none of the 470 non histamine-producing strains produced a product

(Takahashi et al. 2007). The researchers were then able to identify prolific histamine producers

by subsequent single-strand conformation polymorphism (SSCP) analysis (Takahashi et al.

2007). The method of Torres Alves et al. (2002) amplified some unexpected fragments but

when sequenced these were found to match the histidine decarboxylase enzyme of the Gram

positive bacterium Clostridium perfringens. Thus, their method was not producing false positives

but rather successfully identifying bacteria that otherwise might not be expected to be implicated

as histamine producers.


Bjornsdottir et al. (2009) compared modified Niven’s agar with a potentiometric and a PCR

method and although the latter two gave few false positives, they were not able to detect

bacteria that only produced low levels of histamine. These authors concluded that there remains

a need for a simple and straightforward yet sensitive method for detecting histamine-producing

bacteria in seafood and environmental samples.

4.2.4 Methods to determine fish species involved

In order to know where controls need to be applied, it is important to know which fish are

causing outbreaks of histamine poisoning. However, in many outbreaks (e.g. 7 of the 31 in

Table 1) the actual species of fish involved remains totally unidentified and in other cases a

generic term is applied rather than a specific one. For example, 4 of the 31 outbreaks in Table 1

just referred to tuna, which might include any of at least 9 species present in New Zealand

waters (Ayling & Cox 1982) as well as numerous imported species. Lago et al. (2009)

developed a genotypic test (FINS – Forensically Informative Nucleotide Sequencing) that could

be used to determine the species of fish involved in histamine outbreaks. A polymerase chain

reaction-restriction fragment length polymorphism (PCR-RFLP) method was also used to

identify the species of the suspected billfish samples in two Taiwanese outbreaks of histamine

poisoning (Yung-Hsiang et al. 2007b).

4.3 Bacteria responsible

Production of histamine and other biogenic amines correlates with increasing bacterial numbers

(e.g. Wen-Xian et al. 2001), but only a small proportion of the total bacterial flora that grows on

fish can produce histamine (e.g. 12% in iced anchovies (Pons-Sanchez-Cascado et al. 2005a)).

For bacteria to produce histamine, they must produce the exogenous enzyme, histidine

decarboxylase, which converts histidine into histamine. In a review of literature up to 2002 Shin-

Hee et al. (2003a) summarised the bacteria considered responsible for histamine production in

fish. They identified two main groups, enteric bacteria and marine bacteria, but they considered

that enteric M. morganii was the main contributor because of its ability to produce high levels of

histamine.

Recent years have seen great advances in the ready identification of bacterial isolates by

genotypic methods, particularly using PCR amplification for subsequent sequencing of 16S

rDNA. This has led to the recognition of new bacterial species that can cause histamine

production. Until 2000 most bacteria reported as being responsible for histamine poisoning were

mesophiles, mostly of the Enterobacteriaceae family with minor contributions from other groups

such as Pseudomonas. Recent work supporting this finding includes that of Du et al. (2002) who

identified Morganella morganii, Enterobacter agglomerans, Enterobacter intermedium, Serratia

liquefaciens, Proteus vulgaris, as well as Pseudomonas fluorescen as the decarboxylase-

positive bacterial species responsible for histamine production in test tuna fillets.

M. morganii was the most commonly implicated organism, for example, 28% of bacterial

isolates from spoiled Indian anchovies were identified as histamine producers with Proteus

vulgaris, Enterobacter aerogenes and Morganella morganii identified as prolific histamine

producers (Sureelak et al. 2005). Kim et al. (2002b) only found what they described as weak

histamine formers (Hafnia alvei, Photobacterium damsela, Acinetobacter lwoffii, Enterobacter

cloacae, Enterobacter aerogenes, all producing less than 350 mg/kg histamine) on fresh

albacore tuna although the prolific histamine formers (M. morganii producing more than

3000 mg/kg histamine) were found following 3 days at 25°C when counts reached 107 cfu/g.


M. morganii was more common in mackerel and sardines than in tuna (Kim et al. 2003). The

most prolific and prevalent histamine former in Pacific mackerel was M. morganii, followed by

Proteus vulgaris (Shin-Hee et al. 2000; Shin-Hee et al. 2001a). Histamine production by M.

morganii was reported to be maximal for stationery phase organisms (≥106 cfu/g) at 25°C and

the organism did not grow or produce histamine at 4°C (Shin-Hee et al. 2000; Kim et al. 2002a),

results comparable to those found our work (see Section 3.4). M. morganii can also produce

cadaverine, putrescine and phenylethylamine in tuna infusion broth, biogenic amines that have

been proposed to act as potentiators for histamine poisoning (Shin-Hee et al. 2000). However,

working with tuna flesh, Veciana-Nogues et al. (2004) observed that M. morganella produced

cadaverine but not putrescine, although both were observed in bluefish (Pomatomas saltatrix).

M. morganella was most frequently present in the gill followed by the skin but rarely in the

intestine and body cavity. The bacterium was not found in the processing plant, but was

detected on the surfaces of conveyor belts and plastic totes during processing (Kim et al. 2003).

It was considered endogenous to fish (Kim et al. 2003). Although S. liquefaciens showed lower

histamine production than M. morganii in synthetic medium, the reverse was true in a medium

formulated from tuna muscle protein extracts (Guillen-Velasco et al. 2004). This is the reverse of

what we found in our medium derived from kahawai extracts where M. morganii was more

prolific than Serratia (Section 3.4.2). However, as in our work, the authors of that study did

suggest that high histamine production might be related to bacterial stress (Guillen-Velasco et

al. 2004).

Other studies implicating members of the Enterobacteriaceae did not find M. morganii. Min-Ki et

al. (2009) found Enterobacter aerogenes to be the main organism producing large amounts of

histamine in Korean fish although other histamine-producing Enterobacter were also present.

Enterobacteriaceae (Citrobacter freundii, Enterobacter agglomerans, Serratia liquefaciens) were

also the bacteria with the highest histamine-producing activity in Atlantic mackerel (Scomber

scomber) (Merialdi et al. 2001) and most histamine producers in Brazilian shrimp belonged to

the Enterobacteriaceae family (Sousa Andrade et al. 2008). Proteus, Enterobacter, Klebsiella,

Rahnella and Acinetobacter, were identified as histamine producers in Taiwanese sailfish

(Yung-Hsiang et al. 2004). In contrast to other research, showing histamine producers to only

contribute a small part of the microflora, Özogul & Özogul (2005) reported that the majority of

bacterial strains isolated from fresh, spoiled and vacuum or MAP herring produced histamine in

a medium supplemented with histidine. Highest histidine decarboxylase activities were observed

from Klebsiella oxytoca, Hafnia alvei and Proteus vulgaris, which produced 396, 232 and 54

mg/kg histamine, respectively (Özogul & Özogul 2005).

There have also been reports of mesophilic bacteria other than the well recognised

Enterobacteriaceae potentially causing histamine poisoning. Working with mahimahi

(dophinfish) and yellowfin tuna, Allen et al. (2005) isolated the Gram positive Staphylococcus

kloosii as well as Enterobacter cloacae and three other Gram negative bacterial species

capable of producing histamine. These bacteria only produced low levels of histamine and only

at temperatures above 15°C. Despite the presence of histamine-producing bacteria, no

detectable levels were found in the composite fish muscle samples analysed even though they

report 60% of the yellowfin tuna harvested did not meet the US FDA's regulatory HACCP

guidelines for temperature reduction (Allen et al. 2005). In line with our work (Section 4.1) this

suggests that, although these organisms are capable of producing histamine, in practice they

may not do so in seafood. In contrast to the findings of Allen et al. (2005), Pons-Sanchez-

Cascado et al. (2005a) found that although E. cloacae produced putrescine and cadaverine, it

did not produce histamine. Similarly, none of the Gram-positive catalase-positive cocci that they

isolated from iced anchovies showed aminogenic activity, although all enterococci isolates did


(Pons-Sanchez-Cascado et al. 2005a). Although most commonly associated with perfringens

food poisoning, Clostridium perfringens can also produce histamine (Torres Alves et al. 2002).

While confirming M. morganii as the most prolific histamine producer in tuna, Economou et al.

(2007) also found that Staphylococcus hominis, Enterococcus hirae and Klebsiella oxytoca

produced high levels of histamine. In dried milkfish using 16S rDNA sequencing with PCR

amplification, histamine producers were identified as Staphylococcus sciuri subsp. sciuri,

Serratia grimesii, Bacillus cereus and Raoultella ornithinolytica (Yung-Hsiang et al. 2006). R.

ornithinolytica was a potent histamine-former capable of producing more than 800 mg/kg of

histamine in broth in the presence of 1.5% or 3.5% NaCl and this was suggested as the

causative agent of an outbreak in dried milkfish (Yung-Hsiang et al. 2007a).Although Bacillus

subtilis was the only histamine producing bacteria isolated from marlin fillets implicated in an

outbreak researchers suspected that other bacteria might have been involved because B.

subtilis only produces low levels of histamine (Chen et al. 2010). K. oxytoca produced

cadaverine over a wide range of temperatures but only produced histamine at room

temperatures (Veciana-Nogues et al. 2004). Hsien-Feng et al. (2008) identified Staphylococcus

carnosus as a histamine producer in salted mullet roe while Enterobacter spp., Pantoea

agglomerans, Klebsiella variicola and Serratia marcescens were implicated in tuna dumplings

(Hwi-Chang et al. 2008). Hsiu-Hua et al. (2009) identified Enterobacter aerogenes, Citrobacter

sp., Staphylococcus xylosus, Staphylococcus sciuri, Bacillus thuringiensis, Citrobacter freundii,

Klebsiella pneumoniae and Enterobacter cloacae as histamine-producing bacteria found in

dried monkfish. Ben-Gigirey et al. (2000) isolated Stenotrophomonas maltophilia strains from

tuna that exhibited histidine carboxylase activity although only low levels (<25 mg/kg) of

histamine were produced. Stenotrophomonas maltophilia was previously classified as a

Pseudomonas species so could possibly be one of the organisms classified in our study as a

Pseudomonad not likely to contribute significantly to histamine production in practical situations

(Section 3.4). Silva et al. (Silva et al. 2002) found that most histamine-producing bacteria

isolated from Portuguese vacuum-packed, cold smoked fish tended to produce histamine at

25°C but not at 5°C although histamine production by lactic acid bacteria was similar at both

temperatures.

The source of the mesophilic bacteria responsible for histamine production has been shown not

to be from fishing vessels or fish processing facilities (Gingerich et al. 2001). They are normally

considered to be natural parts of the microflora of gills, and guts of saltwater fish that

contaminate the flesh after death with contamination being aggravated if left in the water after

death or during processing (e.g. butchering or filleting) (Food and Drug Administration 2001).

Lokuruka et al. (2006) found that both skin and guts were potential sources of histamine

producing bacteria and contamination from skin was more important than that from gutting in

Atlantic mackerel.

As well as mesophilic bacteria, it has long been recognised that a few psychrotrophic organisms

are implicated (Okuzumi et al. 1982). Recently Danish workers have identified some of these

psychrophiles. Initially they reported the psychrotrophic Photobacterium phosphoreum and a

psychrotrophic Morganella-like organism (later named Morganella psychrotolerans (Emborg et

al. 2006) as being responsible for histamine production in Sri Lankan chilli-marinated tuna when

stored at 1–3°C (Emborg et al. 2005). They also reported both of these organisms as being

responsible for an outbreak from cold smoked tuna (Emborg & Dalgaard 2006) and P.

phosphoreum as being responsible for producing high levels of histamine in garfish stored at

5°C (Dalgaard et al. 2006). P. phosphoreum is well known to be a major spoilage organism of

fish packaged under MAP: although its growth is reduced by CO2, histamine production was

found to be higher in an atmosphere containing 60% CO2/15% O2/25% N2 than in air (Lopez-


Caballero et al. 2002). Although most organisms that produce histamine only do so under

certain conditions (e.g. see Figures 3–6), M. morganii and M. psychrotolerans appear to

produce it whenever present in sufficient numbers and where histidine is present as a substrate.

On this basis, Dalgaard and co-workers have modelled the growth and histamine production of

M. morganii under different temperature regimes (Emborg & Dalgaard 2008a) and M.

psychrotolerans under different temperatures, atmospheres, salt levels and pH (Emborg &

Dalgaard 2008a): these two models are freely available in user friendly software (Dalgaard

2009). The combined temperature models for the two organisms show M. psychrotolerans to be

the main histamine producer under refrigeration conditions while M. morganella is the main

organism responsible under temperature abuse situations (Dalgaard 2009).

The histamine-producing capability of P. phosphoreum has been attributed to two histidine

decarboxylases (one constitutive and one inducible enzyme) that have been isolated and

separated from cell-free extracts using GC (Morii & Kasama 2004). Although cell-free extracts of

the constitutive and inducible enzymes had higher activity in cultures grown at 7°C, 5% NaCl

and pH 7.5 and 6.0 respectively, the activity of the enzymes were optimum at 0% NaCl,

temperatures of 30°C and 40°C respectively and at pH of 6.5 and 6.0 respectively. The

differences in these two enzymes extended the histidine decarboxylase activity range of P.

phosphoreum to a wide range of conditions (Morii & Kasama 2004).

Zhihua et al. (2009) found that M. morganii and P. phosphoreum behaved differently with regard

to diffusion of histamine in tuna. Tuna inoculated with M. morganii and incubated at 25°C

produced high levels of histamine (4000 mg/kg) at the point of inoculation but lower levels

(ca 2000 mg/kg) at points 0.5–2.5 cm away from the point of inoculation. In contrast P.

phosphoreum produced 1000–2000 mg/kg in all positions. At 20°C M. morganii produced less

than 2000 mg/kg at the point of inoculation and less than 100–1000 mg/kg at more distant

points while P. phosphoreum produced at 2000 mg/kg at the point of inoculation and 200–1000

mg/kg at more distant points. The researchers postulated that histamine production was

preceded by the spread of bacteria, but did not confirm whether diffusion of exogenous

enzymes could have caused a similar result. Each bacterial species showed a pattern of

increasing histamine levels with time followed by some decreases (Zhihua et al. 2009). This

decrease may be due to the action of histamine oxidases that can break down histamine.

Bermejo et al. (2003) reported that the organisms producing the greatest amount of histamine in

jack mackerel were Proteus vulgaris, Aeromonas hydrophila and Photobacterium damsela: at

least the latter two are psychrotrophic bacteria. They report that histamine production was

proportional to the growth rate of the whole bacterial population when measured at 25, 15 and

5°C (Bermejo et al. 2003, 2004). This reflects our New Zealand work where we found total

bacterial counts were a reasonable indicator of risk of high histamine levels (Fletcher et al.

1995). Bermejo et al. found histamine levels to increase and then decrease after long periods of

storage, presumably due the actions of amine oxidases (Bermejo et al. 2004).

The halophilic Tetragenococcus muriaticus was shown to be able to produce histamine under

the low pH and high salt conditions found in fish sauce (Kimura et al. 2001). Pantoea spp.,

Enterobacter cloacae and P. agglomerans were also identified as histamine-producing bacteria

in Taiwanese salted mackerel (Yung-Hsiang et al. 2006). Satomi at al. (2008) identified another

Tetragenococcus species, T. halophilus as producing histamine in fish sauce and further

showed that its histidine decarboxylase gene was located on a plasmid. They conclude that

histidine decarboxylase genes could be encoded on transformable elements of lactic acid


bacteria. In contrast Lakshmanan et al. (2002) did not find any histamine-producing bacteria

among the halophilic bacteria that they isolated during salt-drying of sardines.

4.4 Products and handling practice effects

Products that are implicated in histamine poisoning usually contain levels of more than 500

mg/kg histamine in their flesh (Dalgaard et al. 2008). However, some incidents have been

caused by fish with less than 200 mg/kg histamine, e.g. a recent outbreak in Japan was

attributed to histamine where only 4–74 mg/kg histamine were recorded (Kan et al. 2000).

Dalgaard et al. (2008) suggest that this apparent discrepancy might be explained through

sampling protocol: in most cases the actual portion of fish being consumed is not tested for

histamine but rather other fish or portions from the same batch. They cite the work of Frank et al

(1981) showing that whilst the anterior dorsal region of tuna might have a histamine level of

1020 mg/kg, a portion from the tail section might only contain 29 mg/kg. Work on other species

has shown similar levels of variation (Dalgaard et al. 2008). The question as to why dietary

histamine causes food borne illness when consuming pure histamine is not toxic was reviewed

by Lehane & Olley (2000), Mavromatis & Quantick (2002) and Dalgaard et al. (2008) with

different conclusions (see Section 4.1). One hypothesis is that seafood products contain a mast

cell degranulator and that it is not the histamine in seafood per se that is directly contributing to

the condition while another is that the presence of other biogenic amines found in seafood

potentiates the toxicity of histamine by inhibiting the normal histamine metabolising enzymes.

The latter hypothesis has been supported by the fact that patients taking the drug isoniazid,

which is known to inhibit histamine-metabolising enzymes, had increased sensitivity to

histamine in food (Miki et al. 2005).

Tuna continues to be the main cause of histamine poisoning internationally, often as a result of

imported product, for example tuna from Indonesia and Vietnam causing outbreaks in the USA

(Davis et al. 2007). There was an unseasonal increase in outbreaks associated with tuna in the

UK in the 6 months between December 2004 and June 2005 with 16 reported outbreaks

compared to 56 for the 12-year period between 1992 and 2004 when outbreaks were more

frequent in the summer (Anon. 2005). These outbreaks appeared to be due to wholesale tuna

(often vacuum packed) being temperature-abused at catering premises. In a 1998 tuna

associated outbreak in Pennsylvania, although the tuna may have had some temperature abuse

before processing, indications were that the scombrotoxin formed at the restaurant where it was

consumed (Maher et al. 2000). Processed tuna has also been implicated a number of US

poisoning cases involving tuna burgers as well as tuna salad and fillets (Becker et al. 2001). For

the most part these cases are also related to temperature abuse by restaurants (Becker et al.

2001). Elevated levels of histamine were recorded in skipjack tuna burgers stored for 4 weeks at

5°C (Mahendradatta 2003).

Other well known scombroid and non-scombroid fish that accumulate high levels of histamine

include bonito (Sarda sarda); mackerel (Scomber japonicus peruanus) and dophinfish

(Coryphaena hippurus) (Gonzaga et al. 2009). Dophinfish are found in New Zealand as are

species of the other two genera. Anchovies (Engraulis encrasicolus) and sardines (Sardina

pilchardus) developed high levels of histamine (>1000 mg/kg) within 24 h at 25°C although only

38 mg/kg developed in mackerel (Visciano et al. 2004; Visciano et al. 2007). Canned anchovies

were also reported to occasionally contain histamine levels above 1000 mg/kg with 20% of

samples exceeding 500 mg/kg (Kim et al. 2004; Hyoungill et al. 2005).


A survey of 17 South African seafood species showed that Thyrsites atun (snoek known as

barracouta or snake mackerel in New Zealand) and Seriola lalandi (yellowtail) are the primary

fish species in South Africa posing a histamine poisoning risk for consumers (Auerswald et al.

2006). Both of these species contained elevated levels of free histidine, and yellowtail was also

identified in several histamine poisoning outbreaks in South Africa. With a measured histidine

level of 250 mg/kg, we listed barracouta as of a lower risk when considering which species had

potential to cause histamine poisoning in New Zealand (Fletcher et al. 1995). We note that a

species related to South African yellowtail (Seriola grandis – kingfish) has been implicated in

New Zealand cases (Foo 1975a) and another related species, Seriola hippos (Samson fish from

Australia), occasionally occurs in New Zealand waters (Ayling & Cox 1982). The level of

histamine exceeded the legal limit (50 mg/kg) in eel (Anguilla anguilla) stored without ice after

6–7 days and, in ice, after 13–14 days of storage, when eels were rejected by the sensory

panel. Thus, native eels may be another potential source of histamine poisoning in New

Zealand.

Two outbreaks of histamine poisoning were caused by species of billfish (Makaira nigricans and

Xiphias gladius) in Taiwan with each product containing histamine levels greater than 1500

mg/kg (Yung-Hsiang et al. 2007b). These game fish species (known locally as blue marlin and

broadbill swordfish respectively) also occur in New Zealand: presence of histamine-producing

bacteria in these species may account for some of the outbreaks attributed to swordfish and

marlin in New Zealand (Section 2). In another reported outbreak in Taiwan, the implicated blue

marlin only contained about 450 mg/kg histamine (Chen et al. 2010). Histamine was recorded at

levels of up to 288 mg/kg in sailfish (Istiophorus platypterus) in Taiwan (Yung-Hsiang et al.

2004). This game fish species occasionally occurs in northern New Zealand (Ayling & Cox

1982). Milkfish (Chanos chanos) also caused an outbreak in Taiwan (Yung-Hsiang et al. 2007a)

and was a better substrate for histidine decarboxylase than sailfish (Yung-Hsiang et al. 2005c),

but this genus is not known in New Zealand (Ayling & Cox 1982).

Histamine at levels greater than or equal to 50 mg/kg was detected in10% of Japanese retail

seafood with levels reaching 3400 mg/kg (Kan et al. 2005). Of the positive samples, 35% were

of semi-dried round and split sardines. Venezuelan results showed that some sardine batches

arriving at the processing plants contained up to 5 mg/kg histamine due to temperature abuse

during transportation (Rosas & Reyes 2009). Control of time and temperature during

transportation and processing was recommended to manage this. Only 9% of tested Austrian

retailed fish products exceeded histamine levels of 50 mg/kg (Paulsen et al. 2000) and none

exceeded their national limits of 200 mg/kg (Anon. 1993). In Greece 15% of tested retail

samples exceeded 50 mg/kg (Vosikis et al. 2008) with highest levels found in herring and

anchovy samples (Vosikis et al. 2008). Temperate Atlantic mackerel (Scomber scombrus)

produced higher levels of histamine than tropical fish (Lokuruka & Regenstein 2004).

Escolar fish (Lepidocybium flavobrunneum) caused an outbreak of histamine poisoning in the

USA: people consuming less than 215 mg histamine experienced fewer symptoms that were of

shorter duration than those consuming more fish and thereby more histamine (Feldman et al.

2005). Escolar has also been recorded as the cause of outbreaks in Denmark along with garfish

(Belone belone belone) and imported tuna products (Dalgaard et al. 2008). Dried milkfish

(Chanos chanos) in Taiwan commonly exceeded acceptable histamine limits with 44% of retail

samples exceeding 500 mg/kg (Hsiu-Hua et al. 2009). At ambient temperatures (32°C) tropical

species of mackerel (Rastrigeller kanagurta), sardine (Sardinella fimbriata) and trevally

(Carangoides armatus) exceeded histamine levels of 50 mg/kg after 12, 15 and 15 h

respectively even though sensory properties remained acceptable (Jeya Shakila et al. 2003).


Tropical parrotfish (Callyodon gutatus), barracuda (Sphyraena japonica) and scavengerfish

(Lethrinus nebulosus) showed no evidence for potential histamine poisoning while skipjack tuna

(Euthynnus pelamis), rabbitfish (Siganus oramin) and little mackerel (Rastrelliger kanagurta) did

(Lokuruka & Regenstein 2004). Histamine levels in sea bass (Dicentrarchus labrax) fillets

remained below 30 mg/kg during 16 days’ storage in ice (Paleologos et al. 2004). None of these

potentially scombertoxic fish genera occur in New Zealand (Ayling & Cox 1982) but they could

be imported.

The NZFSA (2009) explicitly identifies the following fish species imported into New Zealand as

potentially problematic from a histamine poisoning perspective: tuna (all species), mackerel

(Scomber scombrus, Scomber australasicus, Scomber japonicus), amberjack (yellowtail

kingfish) (Seriola lalandei), mahimahi (Coryphaena hippurus), bluefish (Pomatomas saltatrix),

sardine including pilchard (Sardinia pilchardus, Sardinops spp., Sardinella spp.) and herring

(Clupea harengus, Clupea pallasii). From the review above at least escolar, garfish, swordfishes

and billfishes should be added to this list.

Fish such as salmon, which contain low levels of histidine, do not develop high levels of

histamine, even if they contain high levels of histamine-producing bacteria such as P.

phosphoreum (Emborg et al. 2002). Histamine levels remained low during 33 days’ refrigerated

storage of hake (Merluccius merluccius L.) under different controlled atmospheres (Ruiz-

Capillas & Moral 2001) and when stored in air for up to 24 h at 25°C (Visciano et al. 2004). Sole

also developed very low levels of histamine (Visciano et al. 2004). Seer fish (Scomberomorus

spp.) are similarly reported to only develop low levels (<4000 mg/kg) of histamine (e.g.

Scomberomorus commersonii developed less than 100 mg/kg in 10 days at 5°C (Jeya Shakila

et al. 2005b)) and therefore to not cause histamine poisoning compared to skipjack, which

develops high levels (>10,000 mg/kg) (Thadhani et al. 2002). Although histamine-producing

bacteria have been found in a number of freshwater fish (Ferraz de Arruda Silveira et al. 2001),

low levels of histidine substrate in these fish mean that it is considered unlikely that they will

ever be the cause of histamine poisoning. In our work (Section 3.1.1) we came to similar

conclusions: only New Zealand fish with histidine levels above 10,000 mg/kg had caused actual

outbreaks of histamine poisoning. However, we suggested fish that contained histidine at

between 2000 and 10,000 mg/kg may have potential to cause histamine poisoning and,

subsequently, trevally in which we measured histidine at 6300 mg/kg has caused an outbreak

(Table 1). In contrast to the above, Kim et al. (2002a) found that M. morganii inoculated on to

salmon (species not specified) produced histamine at levels of up to 4500 mg/kg and Jeya

Shakila & Vasundhara (2002) also found unacceptable levels of histamine to develop in Indian

freshwater carp after 6–12 h at 30°C or 3–5 days at 5°C. Levels of histidine were higher in the

white muscle of dophinfish and tuna than the red muscle (Antoine et al. 2001), which agrees

with our findings in New Zealand fish (Fletcher et al. 1995)

Korean retail fish, squid and shellfish all contained low levels of histamine (<50 mg/kg) (Min-Ki

et al. 2009). Qing-Xi et al. (2007) also found low histamine levels in squid and white prawn

during refrigerated storage. However, Chinese mitten crabs were reported to contain up to 180

mg/kg histamine after 24 h at 20°C (Yanshun et al. 2009) so under some circumstances

histamine can exceed regulatory levels and might become toxic to humans.

Processed specialty fish products can also develop increased levels of histamine. These include

marinated sardines (Gokoglu 2003; Gokoglu et al. 2003) and anchovies (Olgunoglu et al. 2009),

anchovy paste (Pirazzoli et al. 2006), brined Spanish mackerel (Orawan & Pantip 2000), salted

mackerel (Yung-Hsiang et al. 2005a), salted roe (Hsien-Feng et al. 2008), missoltini (salted air


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


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


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


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.


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


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


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).


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


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.


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