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Perspective
Fly Transmission of Campylobacter
Gordon L. Nichols*
*Health Protection Agency, London, United Kingdom
Appendix. Supplementary Information
Temperature
Data
Temperature data were acquired from the British Atmospheric Data Centre
(BADC), the Natural Environment Research Council's (NERC) Designated Data
Centre for the Atmospheric Sciences based at the Rutherford Appleton Laboratory
in Oxfordshire, part of the Central Laboratory of the Research Councils.
Data are available on-line through a World Wide Web interface (http://badc.nerc.ac.uk)
by prearranged agreement. Data were collated for the period 1989–1999,
with 5 locations selected for each region to provide overall coverage
of the region (except London, which had only 2 centers with data available
for the given time period). Location of temperature stations is shown
in the Figure.
There were a total of 47 sites. Some of the data series were missing
data points. The maximum, minimum, and average temperatures were determined
for all days between January 1, 1989, and December 31, 1999. Maximum temperatures
across all sites were used to calculate the presumptive minimum Musca
domestica larval development times.
Methods
The data represent patients who had fecal specimens examined by a microbiology
laboratory in England and Wales between 1989 and 2003 where Campylobacter
was isolated from the sample. Data were acquired through well-described
surveillance processes, and analysis was conducted in Microsoft Access
and Excel (Microsoft Corp., Redmond, WA, USA). Daily cases were based
on the patient specimen date, and a 7-day rolling mean was used to eliminate
the weekly cycles that reflect reduced patient sampling on weekends.
Hypothesis generation was performed through a systematic review of known
and suggested causes of Campylobacter infection, particularly reflecting
on changes in these risks over the period of May and June and assessing
their credibility as biological drivers for the observed seasonality.
Cities and
Towns Included in Figure 2
S1, London; S2, Birmingham; S3, Bristol; S4, Nottingham; S5, Sheffield;
S6, Manchester; S7, Leeds; S8, Leicester; S9, Reading; S10, Plymouth;
S11, Portsmouth; S12, Colchester; S13, Bradford; S14, Southampton; S15,
Poole; S16, Preston; S17, Cardiff; S18, Chelmsford; S19, Norwich; S20,
Ipswich; S21, Truro; S22, Oxford; S23, Shrewsbury; S24, Dudley; S25, Taunton;
S26, Newport; S27, Cambridge; S28, Newcastle; S29, Chester; S30, Gloucester;
S31, Swindon; S32, Chertsey; S33, Coventry; S34, Welwyn; S35, Frimley
Park; S36, High Wycombe; S37, Slough; S38, Exeter; S39, Swansea; S40,
Luton; S41, Torquay; S42, Derby; S43, York; S44, Worcester; S45, Northampton;
S46, Bishops Stortford; S47, Hull; S48, Basildon; S49, Stoke-on-Trent;
S50, Worthing; S51, Stafford; S52, Harrogate; S53, Hereford; S54, Halifax;
S55, Sunderland; S56, Chesterfield and N Derbyshire; S57, Lincoln; S58,
Ashford Kent; S59, Stockport; S60, Blackpool; S61, Maidstone; S62, Liverpool;
S63, Bangor; S64, Llandough; S65, Lancaster; S66, Sutton Coldfield; S67,
Aylesbury; S68, Grimsby; S69, Doncaster; S70, Peterborough; S71, Brighton;
S72, Gateshead; S73, Kettering; S74, Southend; S75, Rhyl; S76, Cheltenham;
S77, Epsom; S78, Chichester; S79, Carlisle; S80, Milton Keynes; S81, Dorchester;
S82, Durham; S83, Bury; S84, Great Yarmouth; S85, Bury St Edmunds; S86,
Warwick; S87, Salisbury; S88, Wolverhampton; S89, Scarborough; S90, Pontefract;
S91, Bath; S92, Winchester; S93, Bishop Auckland; S94, Watford; S95, Bolton;
S96, Eastbourne; S97, Oldham; S98, North Shields; S99, Burnley; S100,
Ashford Middlesex; S101, Kings Lynn; S102, Warrington; S103, Wakefield;
S104, Keighley; S105, Crawley; S106, Barnstaple; S107, Abergavenney; S108,
Boston; S109, Nuneaton; S110, Northallerton; S111, Wrexham; S112, Macclesfield;
S113, Darlington; S114, Bedford; S115, Basingstoke; S116, Weston Supermare;
S117, Middlesborough; S118, Dewsbury; S119, Sutton-in-Ashfield; S120,
Rochdale; S121, Guildford; S122, Worksop; S123, Wigan; S124, Stevenage;
S125, Bridgend; S126, Rotherham; S127, West Bromwich; S128, Solihull;
S129, Burton-upon-Trent; S130, Haverford West; S131, Carmarthen; S132,
Hemel Hempstead; S133, Stockton-on-Tees; S134, Huddersfield; S135, South
Shields; S136, Barnsley; S137, Whitehaven; S138, Chatham; S139, Blackburn;
S140, Redditch; S141, St Leonards-on-Sea; S142, Grantham and Kesteven;
S143, Ormskirk; S144, Scunthorpe; S145, Canterbury; S146, Kidderminster;
S147, Dartford; S148, Aberystwyth; S149, Hexham; S150, Barrow-in Furness;
S151, Redhill; S152, Margate; S153, Walsall; S154, Ashington; S155, Salford;
S156, Merthyr Tydfil; S157, Stourbridge; S158, Haywards Heath; S159, Banbury;
S160, Hartlepool; S161, Prescot; S162, Otley; S163, Southport; S164, Yeovil;
S165, Llanelli. The number of reported Campylobacter cases per
city and town were based on reports from all laboratories serving the
area and are ordered from highest (S1) to lowest (S165) case numbers.
Results from towns reporting smaller numbers of cases were excluded from
the analysis.
Factors
Linked to Campylobacter Infection
The Appendix Table ( 71
KB, 6 pages) provides evidence for seasonal associations between factors
linked to human Campylobacter infections
or outbreaks.
Appendix Table. Evidence
for seasonal associations between factors linked to human Campylobacter
infections or outbreaks |
|
Risk factor |
Outbreaks |
Evidence for factor causing seasonal increase |
Evidence against factor causing seasonal increase |
|
Chicken/turkey |
(1–7) |
Chicken is the food most commonly contaminated with
Campylobacter. A substantial portion of infection probably
derives from this source (1–6,8–10). Some evidence
shows that Campylobacter contamination of chickens is seasonal. |
Chicken is not the vehicle for most sporadic Campylobacter
infections (8,11,12). Little
evidence exists that the seasonal differences in Campylobacter
in chickens are sufficient to drive the seasonality of human disease
(13–18). |
Salads and fruit |
(19–21) |
Untreated leaf salads and soft fruits might be potential
sources of human campylobacteriosis (9,19–21)
because these raw products are eaten without any heat treatment. |
In most of the outbreaks involving salad items,
cross-contamination from contaminated raw foods was thought to be
involved. While seasonal import of fresh fruit or vegetables from
different countries might represent a potential source of infection
it would be surprising if this manifested itself as an annual nationwide
outbreak across the whole of England and Wales while remaining refractory
to epidemiologic investigation. Fly transmission from animal feces
may be important. |
Cross-contamination from raw meats to ready-to-eat
foods |
(9) |
Cross-contamination from raw meats to ready to eat
foods within kitchens and retail premises probably contributes significantly
to Campylobacter infection. |
Why cross-contamination should be strongly influenced
by the season is unclear, unless levels of raw meat contamination
change with the seasons. |
Unpasteurized or inadequately pasteurized milk |
(6,22–33) |
Unpasteurized or badly pasteurized milk can be a
source of Campylobacter infection (6,23,26,29,33–36).
Milk could cause the seasonality if the numbers of Campylobacter
in raw milk changed with the season and other critical control points
in milk production (pasteurization) are not tightly maintained.
Infections related to consumption of unpasteurized milk appear to
be seasonal, with a peak in May, which suggests seasonal changes
in the Campylobacter contamination of unpasteurized milk. |
No evidence shows that the seasonality of human
disease is largely due to unpasteurized milk because this product
is not commonly consumed. No evidence shows that pasteurization
varies substantially by season. |
Birds |
(37,38) |
Campylobacter is common in birds. Migratory
birds result in large seasonal changes in the inputs to the environment
from bird feces and could contribute to human Campylobacter
exposure (39). Migratory birds could be a seasonally
changing driver to human disease (40). The main
likely exposure route if this were the case would be direct contact
with contaminated bird feces in the garden, contamination of field-grown
fruit and vegetables and contamination of source waters for drinking.
Bird-pecked milk is a recognized route by which Campylobacter
infection can be acquired (37,38). The contamination
is thought to result from birds feeding consecutively on cow feces
and milk in bottles. The infections related to bird-pecked milk
appear to be seasonal in distribution with a marked increase in
May (41). |
Bird-pecked milk is unlikely to be the cause of
the worldwide seasonal distribution of Campylobacter infections.
Fly transmission from bird feces, particularly farmed poultry, may
be important. Evidence from extensive monitoring of ready-to-eat
foods sampled at retail businesses suggests little evidence of Campylobacter
contamination (Little, pers. comm.). |
Barbecue |
(1) |
Barbecue use might be a contributing factor to the
total Campylobacter infection because standards of food safety
associated with barbecue use are likely to be poorer (1,42,43).
Case-control studies have found associations between barbecue use
and sporadic Campylobacter infection (44,45). |
Barbecue use on its own is unlikely a big enough,
or seasonal enough, driver of disease to account for seasonal changes
in incidence. |
Food packaging |
|
The packaging around chickens is commonly contaminated
with Campylobacter, which may represent a source of some
infections through cross-contamination. |
Strong seasonal changes in the extent of this contamination
would have to exist for this factor to affect the disease epidemiology,
and no evidence for these changes exists. |
Food handlers/hygiene |
(46–50) |
Infected food handlers might represent a source
of infection in catering premises. |
Infections in food handlers probably are seasonal,
reflecting the seasonality of Campylobacter in general, but
they are probably not the driver for the overall seasonality. |
Food, stir-fried |
(2) |
Stir-fried food may be contaminated through inadequately
cooking raw ingredients or cross-contamination. |
A seasonal change in the contamination of raw ingredients
would need to exist to explain the epidemiology. |
Flies |
|
Flies provide a biological explanation for the spring
increase in Campylobacter cases through the increase in fly
numbers. Campylobacter has been isolated from flies, and
the low infectious dose required to cause human disease would make
this route credible. Historical records link “summer diarrhea” to
flies. |
Little hard evidence exists for this transmission
route. |
Mains drinking water |
(28,51–60) |
|
With mains water supplies, the relatively even distribution
of seasonal changes in the distribution of Campylobacter
cases suggests that any contamination of public supplies must be
systemic (a generic problem with all supplies) or a much bigger
regional difference in the incidence would be seen. Potential seasonal
differences in water quality that could explain why treatment might
not prevent sporadic Campylobacter infection through mains
water (e.g., viable noncultivable Campylobacter in chlorine-resistant
protozoa) are not supported by evidence. The rarity of outbreaks
associated with public water supplies suggests that drinking water
is not a substantial source of Campylobacter infection. |
Private drinking water supplies/untreated surface
water, rain water, or well water |
(6,59;61–70) |
Waterborne infection associated with private water
supplies can result in outbreaks of infection because many people
drink the contaminated water (71). Campylobacter
is the most common organism causing these outbreaks. A seasonal
change in water quality could occur. |
Seasonal changes in water contamination should trigger
outbreaks rather than a national increase in sporadic disease. The
comparative rarity of outbreaks associated with private supplies
suggests that this source does not substantially contribute to the
total illness that is seen to change dramatically with the season.
Given the influence of surface water on the microbiologic quality
of private water supplies, we expect that the seasonal occurrence
of Campylobacter might be more influenced by rainfall than
time of year, which does not appear to happen. |
Bottled water |
|
In a case-case study of Campylobacter, people
with C. coli infection were more likely to have drunk bottled
water than were those with C. jejuni infection (72).
Natural mineral water is not disinfected and could be a widely dispersed
product that experiences seasonal changes in contamination. |
Sources of water that are used to produce natural
mineral water and other bottled waters are relatively well protected.
These groundwaters are unlikely to be contaminated with Campylobacter.
If bottled water consumption is a risk factor, it should come up
as such in analytic epidemiologic studies of Campylobacter
infection. It is unclear why the seasonal pattern of infection should
be so constant both geographically and annually if bottled water
contamination is such a substantial contributor to human disease. |
Pools, lakes, and streams |
|
Potential exists for illness after swallowing contaminated
recreational water (73–76). Water sports in natural
waters can be a source of exposure. If the contamination of water
with Campylobacter is seasonal, then any seasonality in this
group could be linked to either changes in water quality or behavior. |
Illness associated with recreational water activity
has not been established, and this is unlikely to be the source
of the spring increase in campylobacteriosis. Little evidence shows
that the change in recreational water activity in the spring is
enough to explain the seasonal change in Campylobacter cases. |
Within-family transmission |
(77) |
Person-to-person transmission can occur. |
No obvious reason explains why within-household
transmission of Campylobacter should be seasonal, given that
personal hygiene practices are not likely to change substantially
over a matter of weeks. |
Domestic catering |
|
Domestic food preparation may contribute to human
Campylobacter disease. |
Fly transmission within kitchens may contribute
to transmission, and this would likely be seasonal. Little else
within the kitchen environment, other than the contamination of
raw food ingredients, is likely to vary seasonally. |
Nursery/childcare/school |
(78,79) |
As Campylobacter is common in children, transmission
may occur within the childcare setting. |
No evidence shows that infections in childcare are
common or that they vary through the year. |
Nosocomial transmission |
(80) |
|
Nosocomial transmission cannot account for the national
seasonal increase in cases. |
Pets |
|
Pets, particularly kittens and puppies, have been
postulated as a source of Campylobacter. Canine births, as
recorded in Kennel Club and Guide Dogs for the Blind Association
records, show a strong seasonal distribution, and this factor has
been proposed as a driver for human disease (81). |
Little evidence shows that the seasonal change in
Campylobacter is directly related to pets, although fly transmission
from animal feces may be important. |
Farm animals |
(82) |
Campylobacter strains isolated from cattle
have been linked to strains from human infections (83,84).
Cattle and sheep represent a reservoir of Campylobacter (85,86),
and milkborne outbreaks (6,23,26,29,33–36)
suggest that other routes may occur. Fecal shedding by sheep may
be more frequent around lambing (87). Seasonal
differences in Campylobacter infections have also been demonstrated
in rhesus monkeys, other agricultural animals, and birds (15,16,88–91). |
Any seasonality of Campylobacter infection
or colonization in animals could cause seasonality in humans, but
this seasonality is most likely to result from the contamination
of food. Fly transmission from animal feces may be important. |
Farm visits |
(92) |
Visits to farms can expose children to common zoonotic
enteric pathogens, including Campylobacter. |
Any seasonality of farm visits is unlikely to contribute
to the seasonal distribution of all cases. |
The countryside |
|
Direct environmental exposure could occur through
walking in the country. |
This activity may be seasonal but is unlikely to
contribute to the strong seasonal distribution of cases. |
Travel |
|
Campylobacter has been linked to overseas
travel (93–95), including military service (96,97),
and probably represents a significant percentage of all cases of
travelers' diarrhea (98–101). In some countries,
>50% of Campylobacter cases may be linked to foreign travel
(102) |
The seasonality of Campylobacter does not
follow the seasonality of travel abroad. |
Weather/climate |
|
In some developing countries a higher incidence
was seen in the rainy season (103,104), which
suggests flies might be contributory. Although Campylobacter
is more common during the summer months and has been linked to temperature
(105), no direct relationship was seen between
temperature and cases of human disease. The different seasonal distribution
in different countries appears to be partly temperature-related |
Little evidence shows that Campylobacter
is associated with rainfall. There was no association between thermophilic
Campylobacter in lambs at slaughter and rainfall (89).
The main seasonal driver for Campylobacter infection is not
likely to be rainfall itself, since the increase appears to occur
annually, irrespective of when most rain falls. |
Immunologic response |
|
The immunologic response to Campylobacter
exposure could change throughout the year. This hypothesis has been
studied in male rhesus monkeys (88). A marked
seasonality was seen ,with the frequency of TH1-type cytokine synthesis
in the summer being markedly greater than in the winter, whereas
TH2-type cytokine expression did not vary between the seasons. |
Current evidence suggests that seasonal changes
in immunologic response to Campylobacter infection are unlikely
to account for the major seasonal changes in Campylobacter
incidence. |
|
Download
Appendix Table ( 71
KB, 6 pages).
Appendix
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