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| Journal of the New Zealand Medical Association,
18-August-2006, Vol 119 No 1240
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Flies, fingers, fomites, and food. Campylobacteriosis in
New Zealand—food-associated
rather than food-borne
Warrick Nelson, Ben Harris
Sporadic contamination by flies of individual portions of
food is plausible, but does not account for the clear chicken-consumption
association.
Cows are the most likely source of high environmental
Campylobacter contamination in New
Zealand. It is proposed that flies are indeed the link between environmental
sources and food. Increased fly foraging activity as temperatures rise into
summer increase the opportunity for finger contamination by contact with fly
faecal and regurgitated matter deposited on commonly touched surfaces.
Takeaway meals are a particular risk because of the almost
universal lack of hand hygiene prior to eating, especially chicken meals because
of the high moist food contact and licking of fingers during consumption. Thus
flies, fomites, fingers, and food account for both the observed seasonal pattern
and chicken consumption associations with campylobacteriosis.
New Zealand has a particularly high rate of
campylobacteriosis compared to other OECD countries, with 12,000 to 14,000
notified cases per annum (or 300 cases per 100,000 population per annum).
Campylobacteriosis is the dominant cause of the 15,000
bacterial food-borne illnesses reported each year in New Zealand.1,2 Actual
prevalence for these diseases is commonly estimated to be 10–20 times the
reported rates. As well as gastroenteritis,
Campylobacter can also cause other
illnesses including Guillain-Barré syndrome.
Food-borneCampylobacteriosis is typically a sporadic illness (as
distinct from outbreak clustering). It is reported throughout the year, with
marked summer seasonal peaks (Figure 1).
Figure 1. New Zealand-reported
sporadic campylobacteriosis cases per month with least squares linear regression
fitted (grey bars and dotted line). Chicken meat production in tonnes per annum
with least squares linear regression shown (black bars and line)
 Campylobacter data is from
Environmental and Scientific Research (www.esr.cri.nz),
and chicken data is from Poultry Industry Association of New Zealand (www.pianz.org.nz)
The New Zealand trends, apart from being higher per capita,
are similar to other temperate OECD countries, except the peak month in the
Northern Hemisphere shifts to June or July. About 80% of campylobacteriosis
cases are thought to be by food-borne transmission, but unusually with fewer
than 1% of cases occurring as outbreaks.
Chicken consumption alone has been implicated as the source
in about 40% of cases, and
Campylobacter colonisation of chickens
themselves (both living and prepared in retail packs) is high while also showing
a seasonal pattern of colonisation/contamination.2–9
The association between chicken consumption and human
campylobacteriosis cases appears conclusive. The association is even more
specific to chicken eaten outside the home. Figure 1 suggests that New Zealand
campylobacteriosis cases are increasing at about the same rate as New Zealand
chicken consumption (chicken production in New Zealand is almost entirely for
local consumption, and chickens represent almost all poultry meat consumption).
During the Belgian dioxin crisis of 1999, a significant
decline in campylobacteriosis cases occurred at the same time as poultry meat
consumption dropped leading to the conclusion that about 40% of
campylobacteriosis is associated with chicken consumption.6 A similar marked
reduction in campylobacteriosis was reported in the Netherlands following mass
culling of chickens to eradicate an avian influenza outbreak.10
The lack of outbreak patterns of disease strongly suggests
Campylobacter is not commonly
transmitted by raw food or during food preparation alone. Sporadic cases suggest
a sporadic source or sporadic exposure.
While chicken meat prior to cooking is commonly
contaminated, the sporadic incidence of human cases suggests this is not the
source of most infections. Furthermore, analysis at the serotype strain level is
ambivalent for chicken as the primary source of human campylobacteriosis.3,5
In New Zealand, the primary source of infection is suggested
to be dairy and beef cattle.11,12 New Zealand has high dairy and beef cattle
numbers—rising from 8.8 to 9.6 million in the period 2000–2004 (www.nzmeatstatistics.co.nz accessed
30/11/2005)—or 2.3 animals per capita human population.
Fly transmissionFlies have been suggested as a transmission vector to
account for the striking seasonal incidence of campylobacteriosis.13–15
There is no doubt that flies are physically able to transmit the low infective
dose required for Campylobacter. Flies
have already been directly implicated as vectors in broiler chicken infection,16
but no confirmation for human cases yet exists.
Nichols14 suggests that increased fly breeding rate, and
therefore an increased risk of fly faecal contamination of foods, explains the
seasonal nature of infection. This is not supported by New Zealand data where
the seasonal peak occurs directly during the rise in temperatures into summer
(Figure 2) and not with a delay for fly gestation and breeding.
This is more likely to relate to increased existing fly
foraging activity of adult flies that have survived over winter, in contrast to
chickens (where contamination occurs following consumption of the flies), and
their infection peak occurs later when fly numbers have increased.16
Increased fly foraging activity with consequent increased
opportunity for direct and sporadic food contamination fits the observed
seasonal pattern of campylobacteriosis. However, this does not explain the very
strong association with chicken consumption, and particularly chicken eaten away
from home. Flies are unlikely to contaminate chicken meals specifically.
The opportunity for flies to contaminate takeaway meals is
relatively low compared to barbecued foods, yet these are the meals commonly
implicated following illness.
Figure 2. Sporadic campylobacteriosis for (top to
bottom) Taranaki, Canterbury and Southland District Health Boards
 Raw numbers of cases have been
converted to cases per 100,000 based on the 2001 national Census for normally
resident population in each District. Average monthly temperature for New
Plymouth, Christchurch, and Invercargill are plotted on the right hand side.
Temperature data per National Institute for Water and Atmospheric Research
(www.niwa.cri.nz)
Fomites and fingersThere is therefore another step in the route for
environmental Campylobacter to cause
human disease. Increased fly activity will result in increased fly contamination
on common surfaces through faecal deposits and extracorporeal digestion (fly
spots). Some of these deposits will be on hand rails, door handles, and other
surfaces commonly touched by people.
Campylobacter
deposited on human fingertips in an organic medium has been demonstrated to
remain viable for at least 1 hour,17 and it can be recovered from dry surfaces
24 hours after contamination.18
Fast food meals are typically eaten without eating utensils,
even when eaten in restaurant facilities. Personal observation of diners at such
outlets shows very few diners wash their hands prior to touching food, as noted
elsewhere19.
The specific association with chicken meals may be because
chicken portions eaten with the fingers involve more moist-and-fatty food
contact compared with most other fast foods. Contamination on fingers therefore
has more opportunity to be transferred from the fingers to the mouth compared to
foods eaten with less finger-licking. It is also possible that survey responses
are biased against chicken through prior expectation of chicken as the culprit
food.
Contrary to the findings of Hearnden et al,20 this
fly-mediated food-associated transmission route could prove to be the single
dominant transmission route in New Zealand.
Regional differences in seasonal incidence must take into
account environmental sources of
Campylobacter, fly foraging activity,
and longevity of Campylobacter in fly
deposits on touchable surfaces. These sources are likely to be affected by
temperature, humidity, and rainfall variation, affecting both the environmental
availability of bacteria,21 and through weather impacts on fly and human
activities.
DiscussionFurther research to elucidate a food-association source of
campylobacteriosis will be necessary. Direct sampling of diners’ fingers
at fast food outlets may indicate the validity of fingers as a source of
environmental Campylobacter, although
difficulties in culture may mask it.
Since New Zealand already has a reporting procedure in place
for campylobacteriosis, intervention studies, such as an intensive fly control
programme and hand washing education at fast food outlets, could also be used to
determine the role of this mode of transmission.
This suggested food-associated role via flies and
diners’ fingers is not intended to negate efforts to reduce
campylobacteriosis by other means, especially the risk of outbreak disease
through contamination of foods at source or during preparation. Furthermore,
while 40% of cases are thought to be associated with chicken consumption, the
other 60% of cases must therefore be from non-poultry sources.
New Zealand has the worst per capita statistics for
campylobacteriosis amongst OECD countries. A high level of environmental
Campylobacter availability because of
intensive farming practices (linked with a ready transmission route from rural
to urban areas), coupled with poor food hygiene practices, can go a long way to
explaining this high statistic.
Understanding the source of the disease is key to preventive
practices. Programmes in place to reduce the risk of direct
food-borne transmission must not be
reduced. However, additional steps to reduce
food-associated transmission, resulting
in the sporadic pattern of disease, can be undertaken relatively easily.
ConclusionCampylobacteriosis rates in New Zealand follow similar
patterns as those in other temperate OECD countries. This is a marked seasonal
pattern peaking in early summer, sporadic rather than outbreak pattern of
incidence, and increasing cases per capita with increasing chicken meat
consumption.
The marked seasonal pattern does fit with an explanation as
flies as vectors, and flies are implicated directly as transmission agents for
Campylobacter to chickens. The seasonal
and sporadic pattern does not suggest illness arising directly from contaminated
meat.
The empirical data suggests a more complex ecology. This is
proposed as involving seasonal increased overwintered fly foraging activity
accounting for the seasonal component of disease. The flies bring
Campylobacter organisms from the likely
environmental source (cow faeces) to contaminate fomites by defecation and
extracorporeal digestion.
The diners’ fingers become contaminated by touching
these fomites and an infectious dose is transferred during eating, particularly
as it is common not to wash hands prior to eating a takeaway meal. Chicken meals
are particularly implicated because of the intensive finger contact with moist
food, and finger licking, during consumption.
Author information:
Warrick Nelson, Research and Management Consultant, 888 Management Ltd (a
technical, consulting, and publishing agency), Christchurch; Ben Harris, Medical
Laboratory Scientist and General Manager at Southern Community Laboratories,
Christchurch
Acknowledgements: In
addition to 888 Management Ltd and Southern Community Laboratories, we thank ESR
and NIWA for their supply of relevant data on spreadsheets.
Correspondence:
Warrick Nelson, 888 Management Ltd, PO Box 6393, Upper Riccarton, Christchurch.
Email: warrick.nelson@gmail.com
References:
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