Distribution of
An annual increase in
The annual increase in
Distribution of
Cases of
| Risk factor | Outbreaks | Evidence of seasonality | Credibility as the main seasonal driver |
|---|---|---|---|
| Barbecuing | Yes | Medium | Low |
| Birds | Yes | Strong | Low |
| Bottled water | No | None | Low |
| Chicken | Yes | Medium | Medium |
| Cross-contamination | Yes | None | None |
| Domestic catering | No | None | None |
| Farm visit | Yes | None | None |
| Farm animals | Yes | Weak | Low |
| Flies | No | Strong | High |
| Food handlers | Yes | None | None |
| Food packaging | No | None | None |
| Immunologic response | No | Weak | None |
| Mains supply drinking water | Yes | None | None |
| Nosocomial | Yes | None | None |
| Pets | No | Weak | Low |
| Pools, lakes, streams | No | None | None |
| Private drinking water supplies | Yes | Weak | None |
| Protozoa | No | None | Low |
| Salads and fruit | Yes | Weak | Low |
| Stir-fried food | Yes | None | None |
| The countryside | No | Weak | Medium |
| Transmission in families | Yes | None | None |
| Travel abroad | No | None | None |
| Unpasteurized milk | Yes | Weak | None |
| Weather/climate | No | Medium | Medium |
*Evidence base provided in Appendix.
The seasonal increase in
Disease transmission is hypothesized to occur through small quantities of contaminated material carried on the feet, proboscis, legs, and body hairs or from material regurgitated or defecated by flies. The variety, numbers, virulence and viability of organisms in the contaminated material will differ, and some contamination will include
A number of synanthropic fly species could be involved, including houseflies (e.g.,
Flies contaminated through fecal contact will carry heterogeneous mixtures of organisms, including any pathogens that are present within the feces, and may be able to cause a variety of human infections, including infection by different
Contamination of a range of foods by flies will result in a pattern of infection that will not be amenable to identifying specific vehicles through standard case-control, case-case, or cohort studies, unless specific objective or subjective assessments of fly numbers can be obtained. Fly monitoring will need to be undertaken. An alternative approach could use estimates of fly population numbers based on climatic conditions to compare with data on human
The hypothesis predicts that the
While flies are regarded as important mechanical vectors of diarrheal disease in developing countries, control has largely concentrated on improving drinking water and sewage disposal. In the industrialized world, flies are thought to play a minor role in the transmission of human diarrheal diseases. Immediately intervening in the transmission of
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 (
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
The data represent patients who had fecal specimens examined by a microbiology laboratory in England and Wales between 1989 and 2003 where
Hypothesis generation was performed through a systematic review of known and suggested causes of
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
The
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This hypothesis arose after a lecture by Professor Sandy Cairncross at the Centers for Disease Control and Prevention, Atlanta, in the spring of 2002. I thank Fay Burgess, Radha Patel, Chris Lane, Douglas Harding, and Erol Yousef for help in preparing the data; Jim McLauchlin, Barry Evans, Chris Little, and John Edmonds for critically commenting on versions of the paper; and André Charlett for statistical support.
Temperature station locations.
| 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 | Chicken is not the vehicle for most sporadic |
| 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 | 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 | 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) | Bird-pecked milk is unlikely to be the cause of the worldwide seasonal distribution of | |
| Barbecue | (1) | Barbecue use might be a contributing factor to the total | 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 | 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 |
| 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 | 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 | |
| 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). | 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 |
| Bottled water | In a case-case study of | 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 | |
| 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 | 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 | |
| Within-family transmission | (77) | Person-to-person transmission can occur. | No obvious reason explains why within-household transmission of |
| Domestic catering | Domestic food preparation may contribute to human | 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 | 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 | Little evidence shows that the seasonal change in | |
| Farm animals | (82) | Any seasonality of | |
| Farm visits | (92) | Visits to farms can expose children to common zoonotic enteric pathogens, including | 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 | The seasonality of | ||
| Weather/climate | In some developing countries a higher incidence was seen in the rainy season (103,104), which suggests flies might be contributory. Although | Little evidence shows that | |
| Immunologic response | The immunologic response to | Current evidence suggests that seasonal changes in immunologic response to |
Dr. Nichols is an epidemiologist in the Communicable Disease Surveillance Centre, which is part of the Health Protection Agency in London. His research interests include waterborne diseases, foodborne diseases, cryptosporidiosis, and enteric infections.