Kirsty G Hope, Tony D Merritt, David N Durrheim

Introduction

Campylobacter is the most common cause of bacterial gastroenteritis in Australia.¹ The incubation period is usually between 2 and 5 days but can range from 1 to 10 days.² Symptoms include diarrhoea (often bloody), fever and abdominal pain, and can persist for 7 days or longer.² The infective dose required to cause illness is as low as 500 organisms.^3,4 Despite a high number of notifications, outbreaks caused by Campylobacter are uncommonly detected.^3,5–7

Outbreaks of Campylobacter have regularly been associated with poultry and dairy products, and in recent years the number of outbreaks associated with poultry liver dishes has increased in the United States of America and the United Kingdom.^5,6,8

This article describes a point source outbreak of Campylobacter associated with duck liver parfait with a possible short incubation period; and the review of the literature prompted by the investigation, which identifies short incubation periods as a common feature of point source outbreaks associated with poultry liver consumption.

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Methods

OzFoodNet in Hunter New England was contacted in September 2013 with a report of gastroenteritis amongst guests who attended a wedding reception. A retrospective cohort study was conducted amongst the guests. A standardised questionnaire was completed telephonically by trained interviewers.

A case was defined as any person who consumed food and/or beverages at the wedding who had diarrhoea within 7 days of attending the wedding.

Data analysis was conducted with STATA 11. Univariate analysis included attack rates, P-values, relative risks and 95% confidence intervals.

The NSW Food Authority conducted an inspection of the implicated premises. Although there was no food left-over due to the late notification of the outbreak (35 days after the event), information on ingredients and cooking processes of foods served was obtained.

A literature review was conducted using the search term ‘campylobacter’ in combination with ‘poultry’, ‘duck’, ‘chicken’ or ‘liver’. An extract of outbreaks associated with poultry liver (chicken or duck) was obtained from the Australian OzFoodNet outbreak register. Incubation times recorded in hours were converted to days to 1 decimal point.

This outbreak investigation was conducted under the NSW Public Health Act 2010 and thus ethics approval was not required.

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The outbreak

Contact details were available for 33 of the 50 guests, 30 (91%) of whom completed the questionnaire and 17 met the case definition. The median incubation period was 24 hours (range 5–60 hours) and 12 cases reported an incubation period of less than 24 hours. All cases reported diarrhoea, 12 had abdominal pain, nine had fever, seven had nausea and three had vomiting. The median duration of illness was 6 days. One case was hospitalised. One faecal sample was obtained, which was positive for Campylobacter jejuni. The incubation period for the confirmed case was 2 days.

In a univariate analysis, the only significant association with illness was for the consumption of the entree that contained duck liver parfait (relative risk 4.3, 95% confidence intervals 1.2–15.5). Fifteen of the 17 (88.2%) cases ate the duck entrée.

The environmental investigation indicated that the duck liver was cooked to a maximum internal temperature of less than 70°C. No food samples were available for testing. No illness was identified in staff or in guests attending other functions at the implicated venue.

Review of Campylobacter outbreaks associated with poultry liver dishes

Eight published outbreak reports and 6 additional outbreak records from the OzFoodNet register were reviewed (Table). The median incubation period for Campylobacter outbreaks associated with poultry liver in these outbreaks was typically about 2 days, with individual incubation periods ranging from less than 1 day to 9 days. The incubation period for the 1st confirmed case was available for 9 outbreaks, of which 4 (44%) reported an incubation period of less than 1 day.

Table: Characteristics of Campylobacter outbreaks associated with poultry liver

Vehicle	Jurisdiction	Number of cases	Number attending	Number confirmed Campylobacter only	Number confirmed Salmonella and Campylobacter	Median incubation (days)	Incubation range (days)	Incubation first confirmed case (days)
NA = Not available * Current outbreak.
Chicken liver pâté	South Australia4	15	57	3	0	2	0.3–6	<1
Duck liver pâté	United Kingdom8	18	32	8	0	NA	0.5–3	<1
Chicken liver pâté	United Kingdom9	59	175	5	3	2.	0–6	<1
Chicken liver pâté	Australian Capital Territory	7	Unknown	3	0	1	0.5–3.8	<1
Chicken liver pâté	United Kingdom10	49	102	22	0	2.3	0–5	1
Chicken liver pârfait	United Kingdom3	24	67	13	0	2.3	1–5	1
Duck liver pâté	United Kingdom11	45	77	4	0	2.8	0.4–8.4	1
Chicken liver pâté	Tasmania	44	Unknown	5	0	2	0.6–4.1	1.5
Duck liver pârfait	New South Wales*	17	50	1	0	1	0.2–2.5	2
Chicken liver pârfait	United Kingdom12	11	26	4	0	2.5	0.7–7	NA
Chicken liver pâté	New South Wales	11	34	2	0	1.8	1.3–3.5	NA
Duck liver pâté	Western Australia	65	705	3	3	2.5	0.1–8.1	NA
Chicken liver pâté	Scotland13	48	Unknown	15	0	2	0–9	NA
Chicken liver pâté	Queensland	4	Unknown	1	0	1.6	1.1–2.1	NA
Duck liver pan-fried	Queensland	2	Unknown	2	0	2.7	1–3.5	NA

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Discussion

This review indicates that short incubation periods are a common feature of Campylobacter outbreaks associated with poultry liver dishes. During this outbreak 12 (71%) cases indicated onsets within 24 hours of the function. The review of previous poultry liver related outbreaks indicated that 10 of 14 outbreaks (excluding the current outbreak) had a minimum incubation period of less than a day, with the shortest being 0.1 days. When analysis of the 1st case was limited to confirmed infection only, four of the 9 outbreaks had cases with an incubation period less than 1 day and three had an incubation period of 1 day.

Campylobacter infection in humans usually has a reported incubation period of 2 to 5 days, with some references indicating one to 10 days.² Due to the high levels of Campylobacter potentially present within liver, it is possible infected individuals may have a shorter incubation period due to a large dose.

During this outbreak investigation, it was clear that the internal temperature achieved during preparation of the liver dish was not adequate to kill Campylobacter. Poultry livers should be cooked for 2 to 3 minutes after they reach an internal temperature of 70°C.¹⁴ Inadequate cooking of chicken or duck livers has been associated with numerous Campylobacter outbreaks in Australia and internationally.^4,5,8,10,11 Following a review of outbreaks linked to poultry liver dishes in Australia in 2011,¹⁵ Food Standards Australia New Zealand issued advice on the safe cooking of poultry livers.¹⁴ New Zealand studies have shown that Campylobacter contaminates both the external and internal tissue of livers and that inactivation of Campylobacter is proportional to cooking time.^16–17

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Limitations

The outcome of the initial outbreak investigation that prompted this review is subject to potential recall bias as the investigation did not commence until 35 days after the function had occurred. As not all guests could be contacted (30 out of 50 were interviewed) the possibility of selection bias cannot be excluded.

Many of the outbreaks reviewed only obtained stool specimens from a small proportion of cases and thus the illness reported in some individuals may not have been due to Campylobacter. However, there were confirmed cases in previous outbreaks that had incubation periods less than 1 day. Some studies found cases with mixed infections of Salmonella and Campylobacter. Salmonella can have an incubation period as short as 12 hours, and have similar symptoms, therefore it is possible the short incubation periods were the result of another infection rather than Campylobacter in some instances. Three of the outbreaks reviewed identified cases with mixed infection; two of these had incubation periods of less than 1 day.

Incubation periods of Campylobacter outbreaks associated with other food vehicles were not reviewed as part of this study. Therefore no comparison can be made with other food vehicles.

Conclusion

It is not uncommon to identify cases with short incubation periods (less than a day) in campylobacter point source outbreaks associated with poultry liver consumption. This may result from the potentially high infectious dose in liver. Investigators should not discount suspected gastroenteritis cases with short incubation periods when a poultry liver dish is implicated.

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Acknowledgements

Hunter New England Population Health, OzFoodNet NSW, OzFoodNet network, NSW Food Authority.

Author details

Dr Kirsty G Hope, Epidemiologist, OzFoodNet, Hunter New England Population Health, Wallsend, New South Wales

Dr Tony Merritt, Public Health Physician, OzFoodNet, Hunter New England Population Health, Wallsend, New South Wales

Professor David Durrheim, Director, Health Protection, Hunter New England Population Health, Wallsend, New South Wales

Corresponding author: Dr Kirsty Hope, OzFoodNet, Hunter New England Population Health, Locked bag 10, WALLSEND NSW 2287. Telephone:+61 2 4924 6477. Email: kirsty.hope AT sswahs.nsw.gov.au

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References

1. National Notifiable Disease Surveillance System. Canberra, Australian Government of Health, 2013. [online] Accessed on 15 October 2013. Available from: http://www9.health.gov.au/cda/source/cda-index.cfm
2. Heymann DL ed. Control of Communicable Diseases Manual. 19th edn. Washington D.C: American Public Health Association; 2008.
3. Inns T, Foster K, Gorton R. Cohort study of a campylobacteriosis outbreak associated with chicken liver parfait, United Kingdom, June 2010. Euro Surveill 2010;15(44):pII=19704.
4. Parry A, Fearnley E, Denehy E. ‘Surprise’: Outbreak of Campylobacter infection associated with chicken liver pate at a surprise birthday party, Adelaide, Australia, 2012. Western Pac Surveill Response J 2012;3(4):16–19.
5. Little CL, Gormley FJ, Rawal N, Richardson JF. A recipe for disaster: outbreaks of campylobacteriosis associated with poultry liver pâté in England and Wales. Epidemiol Infect 2010;138(12):1691–1694.
6. Taylor EV, Merman KM, Ailes EC, Fitzgerald C, Yoder JS, Mahon BE, et al. Common source outbreaks of Campylobacter infection in the USA, 1997–2008. Epidemiol Infect 2013;141(5):987–996.
7. Unicomb LE, Fullerton KE, Kirk MD, Stafford RJ. Outbreaks of campylobacteriosis in Australia, 2001 to 2006. Foodborne Pathog Dis 2009;6(10):1241–1250.
8. Abid M, Wimalarathna H, Mills J, Saldana L, Pang W, Richardson JF, et al. Duck liver-associated outbreak of Campylobacter infection among humans, United Kingdom, 2011. Emerg Infect Dis 2013;19(8):1310–1313.
9. Wensley A, Coole L. Cohort study of a dual-pathogen point source outbreak associated with the consumption of chicken liver pâté, UK, October 2009. J Public Health 2013;35(4):585–589.
10. Edwards DS, Milne LM, Morrow K, Sheridan P, Verlander NQ, Mulla R, et al. Campylobacteriosis outbreak associated with consumption of undercooked chicken liver pâté in the east of England, September 2011: identification of a dose-response risk. Epidemiol Infect 2013:142(2):352–357.
11. Young NJ, Day J, Montsho-Hammond F, Verlander NQ, Irish C, Pankhania B, et al. Campylobacter infection associated with consumption of duck liver pâté: a retrospective cohort study in the setting of near universal exposure. Epidemiol Infect 2014;142(6):1269–1276.
12. Farmer S, Keenan A, Vivancos R. Food-borne Campylobacter outbreak in Liverpool associated with cross-contamination from chicken liver pârfait: Implications for investigation of similar outbreaks. Public Health 2012;126(8):657–659.
13. O’Leary MC, Harding O, Fisher L, Cowden J. A continuous common-source outbreak of campylobacteriosis associated with changes to the preparation of chicken liver pâté. Epidemiol. Infect 2009;137(3):383–388.
14. Australian New Zealand Food Standards Agency. Cooking poultry liver dishes safely. [online] Accessed on 14 October 2013. Available from: http://www.foodstandards.gov.au/consumer/safety/poultryliver/Pages/default.aspx
15. Merritt T, Combs B, Pingault N. Campylobacter outbreaks associated with poultry liver dishes. Commun Dis Intell 2011;35(4):299–300.
16. Ministry of Agriculture and Forestry. Bacterial concentrations of poultry offal and in mechanically separated meat products at the processing plant. MAF technical paper No:2011/59. May 2011. Accessed 14 October 2013. Available from: http://www.foodsafety.govt.nz/elibrary/industry/bacterial-concentrations-of-poultry-offal.pdf
17. Whyte R, Hudson JA, Graham C. Campylobacter in chicken liver and their destruction by pan-frying. Lett Appl Microbiol 2006;43(6):591–595.

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