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Volume 11, Number 3—March 2005
Perspective

Fly Transmission of Campylobacter

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Author affiliation: *Health Protection Agency, London, United Kingdom

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An annual increase in Campylobacter infection in England and Wales begins in May and reaches a maximum in early June. This increase occurs in all age groups and is seen in all geographic areas. Examination of risk factors that might explain this seasonal increase identifies flies as a potential source of infection. The observed pattern of infection is hypothesized to reflect an annual epidemic caused by direct or indirect contamination of people by small quantities of infected material carried by flies that have been in contact with feces. The local pattern of human illness appears random, while having a defined geographic and temporal distribution that is a function of the growth kinetics of one or more fly species. The hypothesis provides an explanation for the seasonal distribution of Campylobacter infections seen around the world.

Campylobacter spp. are the most common bacterial causes of diarrhea in England and Wales (1). The epidemiologic features of Campylobacter infection have proved difficult to discover, and extensive strain typing has failed to clarify the main transmission routes. Testable hypotheses must be established to explain available evidence, particularly the reason for the observed seasonality. Relatively few outbreaks of Campylobacter gastroenteritis occur (2), and most cases are sporadic. In case-control and case-case studies of sporadic Campylobacter infections, most cases remain unexplained by recognized risk factors (3,4).

Figure 1

Thumbnail of Distribution of Campylobacter cases per day. When averaged for 1989 to 2002, the epidemic begins at approximately day 130, peaks at approximately day 160, and gradually declines through the rest of the year.

Figure 1. . . Distribution of Campylobacter cases per day. When averaged for 1989 to 2002, the epidemic begins at approximately day 130, peaks at approximately day 160, and gradually declines through the...

Figure 2

Thumbnail of Cases of Campylobacter infection in England and Wales based on the patient specimen date. Figure shows broadly similar changes in patterns of infection across the country as measured by laboratory reporting per town or city (cases as a percentage of the annual total) by day of year. Laboratories were ordered by the total number of cases reported over the 14-year period (Appendix).

Figure 2. . . Cases of Campylobacter infection in England and Wales based on the patient specimen date. Figure shows broadly similar changes in patterns of infection across the country as measured by...

The annual increase in Campylobacter infections in England and Wales begins at approximately day 130 (May 9) and reaches a maximum at approximately day 160 (June 8) (Figure 1). Although this seasonal rise is seen in all ages, it is more marked in children (5). Cases in towns and cities across England and Wales show broadly similar seasonal changes in distribution (Figure 2). The relative geographic uniformity of the increase seen in May of most years has the temporal appearance of an annual national epidemic. Because person-to-person infection within the community is uncommon, it is likely that the epidemic is caused by a single main driver for human Campylobacter infection. The possible seasonal drivers were examined, and only vector transmission by flies appears to provide a convincing explanation for the observed seasonal trends (Table).

The seasonal increase in Campylobacter infections in May and June in England and Wales is hypothesized to reflect an annual epidemic caused by direct or indirect exposure of humans to contaminated material carried by several fly species that have been in contact with human, bird, or animal feces or contaminated raw foods. Flies have been shown to carry Campylobacter and can infect both humans and animals (6–8). Intervention studies have demonstrated diarrheal disease reduction linked to control of flies (9–11), and deaths from diarrheal diseases have been linked to measurements of fly abundance (12). The local pattern of human Campylobacter infection appears random, while having a defined geographic and temporal distribution. This distribution is predicted to be linked to the growth kinetics of 1 or more fly species and their access to environmental sources of Campylobacter in feces or food. The seasonal increase in fly populations results from rainy weather and an increase in temperature that causes the development from egg to fly to occur in days rather than months. Individual flies can lay hundreds of eggs, which can result in a large increase in fly numbers in a short period. Fly numbers fluctuate through the summer and decline in October, but the decline is less dramatic and defined than the spring increase.

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 Campylobacter while others will not. Contamination will be distributed over a variety of food types. Contamination of food by flies could occur at any stage of the food supply chain, but Campylobacter counts within the contaminated material on foods will decrease over time; consequently, most infection will result from contamination close to consumption (e.g., in the domestic or catering environment). Because whether a fly has visited contaminated feces is unknown and how a person becomes infected is uncertain, epidemiologic investigation is difficult.

A number of synanthropic fly species could be involved, including houseflies (e.g., Musca spp., Fannia spp.), blowflies (e.g., Calliphora spp., Lucilia spp.), and other dung-related flies (e.g., Sarcophaga spp., Drosophila spp.) (13). These flies have individual behavioral patterns, ecology, physiology, and temporal and geographic distributions that will influence the likelihood of their being in kitchens, on human or animal feces, and on food. Although Musca domestica is the species most likely to be involved because it is commonly found in houses and food-processing establishments, larger flies (e.g., Calliphora spp.) may be able to transmit larger numbers of Campylobacter.

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 Campylobacter species and types. This fact partially explains the lack of a clear epidemiologic picture arising from Campylobacter typing work. Gastrointestinal disease caused by flies is more likely to involve pathogens with a low infectious dose (e.g., Shigella, Campylobacter, Cryptosporidium, Giardia, Cyclospora, Escherichia coli O157), and some of these could have a seasonal component related to flies. Where high fly populations and poor hygiene conditions prevail, as in disasters or famines, or where pathogens can grow within fly-contaminated food, the potential exists for transmitting pathogens with a high infectious dose (e.g., Vibrio cholerae, Salmonella spp.). The access that flies have to human and animal feces will influence the degree to which they are contaminated with different enteric pathogens.

Figure 3

Thumbnail of Campylobacter cases by week and Musca domestica larval growth times. Campylobacter cases per day are plotted against the minimum M. domestica growth times for the 14 days before the date for weeks from January 1989 to December 1999. The time taken for M. domestica larvae to develop was based on understood growth temperatures (145 days divided by the number of degrees above 12°C, up to an optimum of 36°C) (8). The temperatures were based on a maximum temperature in 47 temperature sam

Figure 3. . . Campylobacter cases by week and Musca domestica larval growth times. Campylobacter cases per day are plotted against the minimum M. domestica growth times for the 14 days before the...

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 Campylobacter infections. This approach has the advantage of being able to use historical climatic and disease surveillance data. The broad relationship between Campylobacter cases and ambient temperature has not been explained in terms of disease causation. The time taken for the larvae of M. domestica to develop (13) was applied to temperature data for England and Wales and has been used to show a strong relationship between Campylobacter cases per week and M. domestica larval development time for 1989 to 1999 (Figure 3). Periods when Campylobacter cases exceed a 7-day average of 170 cases per day occurred when M. domestica larval development time was <3 weeks.

The hypothesis predicts that the Campylobacter infection rates will be higher in persons living close to animal production and lower in urban settings because fly numbers will be lower. Some evidence from the United Kingdom (1,14) and Norway (15) supports this hypothesis. Seasonal changes in Campylobacter incidence that are seen around the world may result from changes in fly populations and flies' access to human and animal feces. Much emphasis on foodborne disease reduction has rightly been on kitchen hygiene, since the low infectious dose of Campylobacter makes cross-transmission from raw meats to ready-to-eat foods a substantial risk in domestic and catering environments. Fly transmission may be the most important source of infection in kitchen transmission routes, and establishments that sell ready-to-eat foods may be sources of Campylobacter, if effective fly control is not in operation. Flies may also be important in transmitting Campylobacter in poultry flocks (16) and between other agricultural animals.

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 Campylobacter gastroenteritis should be possible through increased public awareness and more effective fly control.

Appendix

Supplementary Information
Temperature Data

Figure A1

Thumbnail of Temperature station locations.

Figure A1. . . Temperature station locations.

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 A1.

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 A1

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 Table A1 provides evidence for seasonal associations between factors linked to human Campylobacter infections or outbreaks.

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.

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Acknowledgment

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.

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DOI: 10.3201/eid1103.040460

Table of Contents – Volume 11, Number 3—March 2005

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Gordon L. Nichols, Environmental and Enteric Diseases Department, Communicable Disease Surveillance Centre, Health Protection Agency Centre for Infections, 61 Colindale Ave, London NW9 5EQ, United Kingdom; fax: 44(0)20-8905-9907

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