Skip directly to page options Skip directly to A-Z link
Volume 11, Number 3—March 2005
Perspective

Fly Transmission of Campylobacter

Gordon L. Nichols*Comments to Author 
Author affiliation: *Health Protection Agency, London, United Kingdom

Main Article

Table A1

Evidence for seasonal associations between factors linked to human Campylobacter infections or outbreaks. Download PDF(71Kb, 6 pages).

Risk factor Outbreaks Evidence for factor causing seasonal increase Evidence against factor causing seasonal increase
Chicken/turkey (17–23) Chicken is the food most commonly contaminated with Campylobacter. A substantial portion of infection probably derives from this source (17–22,24–26). Some evidence shows that Campylobacter contamination of chickens is seasonal. Chicken is not the vehicle for most sporadic Campylobacter infections (24,27,28). Little evidence exists that the seasonal differences in Campylobacter in chickens are sufficient to drive the seasonality of human disease (29-34).
Salads and fruit (35-37) Untreated leaf salads and soft fruits might be potential sources of human campylobacteriosis (25, 35-37) 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 (25) 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 (22, 38-49) Unpasteurized or badly pasteurized milk can be a source of Campylobacter infection (22,39, 42, 45, 49-52). 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 (53,54) 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 (55). Migratory birds could be a seasonally changing driver to human disease (56). 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 (53,54). 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 (57). 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 (17) 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 (17,58, 59). Case-control studies have found associations between barbecue use and sporadic Campylobacter infection (60,61). 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 (62-66) 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 (17) 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 (44, 67-76) 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 (22, 75,77-86) Waterborne infection associated with private water supplies can result in outbreaks of infection because many people drink the contaminated water (87). 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 (88). 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 (89-92). 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 (93) 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 (94,95) 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 (96) 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 (97). 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 (98) Campylobacter strains isolated from cattle have been linked to strains from human infections (99,100). Cattle and sheep represent a reservoir of Campylobacter (101,102), and milkborne outbreaks (23, 39,42,45,49-55) suggest that other routes may occur. Fecal shedding by sheep may be more frequent around lambing (103). Seasonal differences in Campylobacter infections have also been demonstrated in rhesus monkeys, other agricultural animals, and birds (31, 32, 104-107). 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 (108) 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 (109-111), including military service (112,113), and probably represents a significant percentage of all cases of travelers' diarrhea (114-117). In some countries, >50% of Campylobacter cases may be linked to foreign travel (118) 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 (119, 120), which suggests flies might be contributory. Although Campylobacter is more common during the summer months and has been linked to temperature (121), 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 (105). 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 (104). 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.

Main Article

References
  1. Tam  CC. Campylobacter reporting at its peak year of 1998: don't count your chickens yet. Commun Dis Public Health. 2001;4:194–9.PubMedGoogle Scholar
  2. Frost  JA, Gillespie  IA, O'Brien  SJ. Public health implications of campylobacter outbreaks in England and Wales, 1995–9: epidemiological and microbiological investigations. Epidemiol Infect. 2002;128:111–8. DOIPubMedGoogle Scholar
  3. Adak  GK, Cowden  JM, Nicholas  S, Evans  HS. The Public Health Laboratory Service national case-control study of primary indigenous sporadic cases of campylobacter infection. Epidemiol Infect. 1995;115:15–22. DOIPubMedGoogle Scholar
  4. Gillespie  IA, O'Brien  SJ, Frost  JA, Adak  GK, Horby  P, Swan  AV, A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses.
  5. Louis  VR, Gillespie  IA, O'Brien  SJ, Russek-Cohen  E, Pearson  AD, Colwell  RR. Temperature driven Campylobacter seasonality in England and Wales. Appl Environ Microbiol. 2005;71:85–92. DOIPubMedGoogle Scholar
  6. Khalil  K, Lindblom  GB, Mazhar  K, Kaijser  B. Flies and water as reservoirs for bacterial enteropathogens in urban and rural areas in and around Lahore, Pakistan. Epidemiol Infect. 1994;113:435–44. DOIPubMedGoogle Scholar
  7. Rosef  O, Kapperud  G. House flies (Musca domestica) as possible vectors of Campylobacter fetus subsp. jejuni. Appl Environ Microbiol. 1983;45:381–3.PubMedGoogle Scholar
  8. Shane  SM, Montrose  MS, Harrington  KS. Transmission of Campylobacter jejuni by the housefly (Musca domestica). Avian Dis. 1985;29:384–91. DOIPubMedGoogle Scholar
  9. Chavasse  DC, Shier  RP, Murphy  OA, Huttly  SR, Cousens  SN, Akhtar  T. Impact of fly control on childhood diarrhoea in Pakistan: community-randomised trial. Lancet. 1999;353:22–5. DOIPubMedGoogle Scholar
  10. Cohen  D, Green  M, Block  C, Slepon  R, Ambar  R, Wasserman  SS, Reduction of transmission of shigellosis by control of houseflies (Musca domestica). Lancet. 1991;337:993–7. DOIPubMedGoogle Scholar
  11. Emerson  PM, Lindsay  SW, Walraven  GE, Faal  H, Bogh  C, Lowe  K, Effect of fly control on trachoma and diarrhoea. Lancet. 1999;353:1401–3. DOIPubMedGoogle Scholar
  12. Niven  J. Summer diarrhoea and enteric fever. Proc R Soc Med. 1910;III(Epidem. Sect.):131–216.
  13. Kettle  DS. Medical and veterinary entomology. 2nd ed. Wallingford (UK): CABI Publishing; 2000.
  14. Skirrow  MB. A demographic survey of campylobacter, salmonella, and shigella infections in England. A Public Health Laboratory Service survey. Epidemiol Infect. 1987;99:647–57. DOIPubMedGoogle Scholar
  15. Kapperud  G, Aasen  S. Descriptive epidemiology of infections due to thermotolerant Campylobacter spp. in Norway, 1979–1988. APMIS. 1992;100:883–90. DOIPubMedGoogle Scholar
  16. Hald  B, Skovgard  H, Bang  DD, Pedersen  K, Dybdahl  J, Jespersen  JB, Flies and Campylobacter infection of broiler flocks. Emerg Infect Dis. 2004;10:1490–2. DOIPubMedGoogle Scholar
  17. Allerberger  F, Al Jazrawi  N, Kreidl  P, Dierich  MP, Feierl  G, Hein  I, Barbecued chicken causing a multi-state outbreak of Campylobacter jejuni enteritis. Infection. 2003;31:19–23. DOIPubMedGoogle Scholar
  18. Evans  MR, Lane  W, Frost  JA, Nylen  G. A campylobacter outbreak associated with stir-fried food. Epidemiol Infect. 1998;121:275–9. DOIPubMedGoogle Scholar
  19. Kessel  AS, Gillespie  IA, O'Brien  SJ, Adak  GK, Humphrey  TJ, Ward  LR. General outbreaks of infectious intestinal disease linked with poultry, England and Wales, 1992–1999. Commun Dis Public Health. 2001;4:171–7.PubMedGoogle Scholar
  20. Murphy  O, Gray  J, Gordon  S, Bint  AJ. An outbreak of campylobacter food poisoning in a health care setting. J Hosp Infect. 1995;30:225–8. DOIPubMedGoogle Scholar
  21. Pearson  AD, Greenwood  MH, Donaldson  J, Healing  TD, Jones  DM, Shahamat  M, Continuous source outbreak of campylobacteriosis traced to chicken. J Food Prot. 2000;63:309–14.PubMedGoogle Scholar
  22. Pebody  RG, Ryan  MJ, Wall  PG. Outbreaks of campylobacter infection: rare events for a common pathogen. Commun Dis Rep CDR Rev. 1997;7:R33–7.PubMedGoogle Scholar
  23. Shandera  WX, Tormey  MP, Blaser  MJ. An outbreak of bacteremic Campylobacter jejuni infection. Mt Sinai J Med. 1992;59:53–6.PubMedGoogle Scholar
  24. Rodrigues  LC, Cowden  JM, Wheeler  JG, Sethi  D, Wall  PG, Cumberland  P, The study of infectious intestinal disease in England: risk factors for cases of infectious intestinal disease with Campylobacter jejuni infection. Epidemiol Infect. 2001;127:185–93. DOIPubMedGoogle Scholar
  25. Centers for Disease Control and Prevention. Outbreak of Campylobacter enteritis associated with cross-contamination of food—Oklahoma, 1996. MMWR Morb Mortal Wkly Rep. 1998;47:129–31.PubMedGoogle Scholar
  26. Layton  MC, Calliste  SG, Gomez  TM, Patton  C, Brooks  S. A mixed foodborne outbreak with Salmonella heidelberg and Campylobacter jejuni in a nursing home. Infect Control Hosp Epidemiol. 1997;18:115–21. DOIPubMedGoogle Scholar
  27. Neal  KR, Slack  RC. Diabetes mellitus, anti-secretory drugs and other risk factors for campylobacter gastro-enteritis in adults: a case-control study. Epidemiol Infect. 1997;119:307–11. DOIPubMedGoogle Scholar
  28. Adak  GK, Cowden  JM, Nicholas  S, Evans  HS. The Public Health Laboratory Service national case-control study of primary indigenous sporadic cases of campylobacter infection. Epidemiol Infect. 1995;115:15–22. DOIPubMedGoogle Scholar
  29. Wilson  IG. Salmonella and campylobacter contamination of raw retail chickens from different producers: a six-year survey. Epidemiol Infect. 2002;129:635–45. DOIPubMedGoogle Scholar
  30. Hanninen  ML, Perko-Makela  P, Pitkala  A, Rautelin  H. A three-year study of Campylobacter jejuni genotypes in humans with domestically acquired infections and in chicken samples from the Helsinki area. J Clin Microbiol. 2000;38:1998–2000.PubMedGoogle Scholar
  31. Hudson  JA, Nicol  C, Wright  J, Whyte  R, Hasell  SK. Seasonal variation of Campylobacter types from human cases, veterinary cases, raw chicken, milk and water. J Appl Microbiol. 1999;87:115–24. DOIPubMedGoogle Scholar
  32. Wallace  JS, Stanley  KN, Currie  JE, Diggle  PJ, Jones  K. Seasonality of thermophilic Campylobacter populations in chickens. J Appl Microbiol. 1997;82:219–24.PubMedGoogle Scholar
  33. Humphrey  TJ, Henley  A, Lanning  DG. The colonization of broiler chickens with Campylobacter jejuni: some epidemiological investigations. Epidemiol Infect. 1993;110:601–7. DOIPubMedGoogle Scholar
  34. Kapperud  G, Skjerve  E, Vik  L, Hauge  K, Lysaker  A, Aalmen  I, Epidemiological investigation of risk factors for campylobacter colonization in Norwegian broiler flocks. Epidemiol Infect. 1993;111:245–55. DOIPubMedGoogle Scholar
  35. Kirk  M, Waddell  R, Dalton  C, Creaser  A, Rose  N. A prolonged outbreak of Campylobacter infection at a training facility. Commun Dis Intell. 1997;21:57–61.PubMedGoogle Scholar
  36. Roels  TH, Wickus  B, Bostrom  HH, Kazmierczak  JJ, Nicholson  MA, Kurzynski  TA, A foodborne outbreak of Campylobacter jejuni (O:33) infection associated with tuna salad: a rare strain in an unusual vehicle. Epidemiol Infect. 1998;121:281–7. DOIPubMedGoogle Scholar
  37. Ronveaux  O, Quoilin  S, Van Loock  F, Lheureux  P, Struelens  M, Butzler  JP. A Campylobacter coli foodborne outbreak in Belgium. Acta Clin Belg. 2000;55:307–11.PubMedGoogle Scholar
  38. Centers for Disease Control and Prevention. Outbreak of Campylobacter jejuni infections associated with drinking unpasteurized milk procured through a cow-leasing program—Wisconsin, 2001. MMWR Morb Mortal Wkly Rep. 2002;51:548–9.PubMedGoogle Scholar
  39. Evans  MR, Roberts  RJ, Ribeiro  CD, Gardner  D, Kembrey  D. A milk-borne campylobacter outbreak following an educational farm visit. Epidemiol Infect. 1996;117:457–62. DOIPubMedGoogle Scholar
  40. Fahey  T, Morgan  D, Gunneburg  C, Adak  GK, Majid  F, Kaczmarski  E. An outbreak of Campylobacter jejuni enteritis associated with failed milk pasteurisation. J Infect. 1995;31:137–43. DOIPubMedGoogle Scholar
  41. Jones  PH, Willis  AT, Robinson  DA, Skirrow  MB, Josephs  DS. Campylobacter enteritis associated with the consumption of free school milk. J Hyg (Lond). 1981;87:155–62. DOIPubMedGoogle Scholar
  42. Kalman  M, Szollosi  E, Czermann  B, Zimanyi  M, Szekeres  S, Kalman  M. Milkborne campylobacter infection in Hungary. J Food Prot. 2000;63:1426–9.PubMedGoogle Scholar
  43. Korlath  JA, Osterholm  MT, Judy  LA, Forfang  JC, Robinson  RA. A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis. 1985;152:592–6. DOIPubMedGoogle Scholar
  44. Lind  L, Sjogren  E, Melby  K, Kaijser  B. DNA fingerprinting and serotyping of Campylobacter jejuni isolates from epidemic outbreaks. J Clin Microbiol. 1996;34:892–6.PubMedGoogle Scholar
  45. Morgan  D, Gunneberg  C, Gunnell  D, Healing  TD, Lamerton  S, Soltanpoor  N, An outbreak of Campylobacter infection associated with the consumption of unpasteurised milk at a large festival in England. Eur J Epidemiol. 1994;10:581–5. DOIPubMedGoogle Scholar
  46. Porter  IA, Reid  TM. A milk-borne outbreak of Campylobacter infection. J Hyg (Lond). 1980;84:415–9. DOIPubMedGoogle Scholar
  47. Robinson  DA, Edgar  WJ, Gibson  GL, Matchett  AA, Robertson  L. Campylobacter enteritis associated with consumption of unpasteurised milk. BMJ. 1979;1:1171–3. DOIPubMedGoogle Scholar
  48. Robinson  DA, Jones  DM. Milk-borne campylobacter infection. Br Med J (Clin Res Ed). 1981;282:1374–6. DOIPubMedGoogle Scholar
  49. Wood  RC, MacDonald  KL, Osterholm  MT. Campylobacter enteritis outbreaks associated with drinking raw milk during youth activities. A 10-year review of outbreaks in the United States. JAMA. 1992;268:3228–30. DOIPubMedGoogle Scholar
  50. Lehner  A, Schneck  C, Feierl  G, Pless  P, Deutz  A, Brandl  E, Epidemiologic application of pulsed-field gel electrophoresis to an outbreak of Campylobacter jejuni in an Austrian youth centre. Epidemiol Infect. 2000;125:13–6. DOIPubMedGoogle Scholar
  51. Djuretic  T, Wall  PG, Nichols  G. General outbreaks of infectious intestinal disease associated with milk and dairy products in England and Wales: 1992 to 1996. Commun Dis Rep CDR Rev. 1997;7:R41–5.PubMedGoogle Scholar
  52. Public Health Laboratory Service Study Group. Cryptosporidiosis in England and Wales: prevalence and clinical and epidemiological features. BMJ. 1990;300:774–7. DOIPubMedGoogle Scholar
  53. Riordan  T, Humphrey  TJ, Fowles  A. A point source outbreak of campylobacter infection related to bird-pecked milk. Epidemiol Infect. 1993;110:261–5. DOIPubMedGoogle Scholar
  54. Stuart  J, Sufi  F, McNulty  C, Park  P. Outbreak of campylobacter enteritis in a residential school associated with bird-pecked bottle tops. Commun Dis Rep CDR Rev. 1997;7:R38–40.PubMedGoogle Scholar
  55. Waldenstrom  J, Broman  T, Carlsson  I, Hasselquist  D, Achterberg  RP, Wagenaar  JA, Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrating birds. Appl Environ Microbiol. 2002;68:5911–7. DOIPubMedGoogle Scholar
  56. Broman  T, Palmgren  H, Bergstrom  S, Sellin  M, Waldenstrom  J, Danielsson-Tham  ML, Campylobacter jejuni in black-headed gulls (Larus ridibundus): prevalence, genotypes, and influence on C. jejuni epidemiology. J Clin Microbiol. 2002;40:4594–602. DOIPubMedGoogle Scholar
  57. Sopwith  W, Ashton  M, Frost  JA, Tocque  K, O'Brien  S, Regan  M, Enhanced surveillance of campylobacter infection in the north west of England 1997–1999. J Infect. 2003;46:35–45. DOIPubMedGoogle Scholar
  58. Butzler  JP, Oosterom  J. Campylobacter: pathogenicity and significance in foods. Int J Food Microbiol. 1991;12:1–8. DOIPubMedGoogle Scholar
  59. Kapperud  G. Campylobacter infection. Epidemiology, risk factors and preventive measures. Tidsskr Nor Laegeforen. 1994;114:795–9.PubMedGoogle Scholar
  60. Ikram  R, Chambers  S, Mitchell  P, Brieseman  MA, Ikam  OH. A case control study to determine risk factors for campylobacter infection in Christchurch in the summer of 1992–3. N Z Med J. 1994;107:430–2.PubMedGoogle Scholar
  61. Kapperud  G, Skjerve  E, Bean  NH, Ostroff  SM, Lassen  J. Risk factors for sporadic Campylobacter infections: results of a case-control study in southeastern Norway. J Clin Microbiol. 1992;30:3117–21.PubMedGoogle Scholar
  62. Fitzgerald  C, Helsel  LO, Nicholson  MA, Olsen  SJ, Swerdlow  DL, Flahart  R, Evaluation of methods for subtyping Campylobacter jejuni during an outbreak involving a food handler. J Clin Microbiol. 2001;39:2386–90. DOIPubMedGoogle Scholar
  63. Olsen  SJ, Hansen  GR, Bartlett  L, Fitzgerald  C, Sonder  A, Manjrekar  R, An outbreak of Campylobacter jejuni infections associated with food handler contamination: the use of pulsed-field gel electrophoresis. J Infect Dis. 2001;183:164–7. DOIPubMedGoogle Scholar
  64. Gent  RN, Telford  DR, Syed  Q. An outbreak of campylobacter food poisoning at a university campus. Commun Dis Public Health. 1999;2:39–42.PubMedGoogle Scholar
  65. Wight  JP, Rhodes  P, Chapman  PA, Lee  SM, Finner  P. Outbreaks of food poisoning in adults due to Escherichia coli O111 and campylobacter associated with coach trips to northern France. Epidemiol Infect. 1997;119:9–14. DOIPubMedGoogle Scholar
  66. Winquist  AG, Roome  A, Mshar  R, Fiorentino  T, Mshar  P, Hadler  J. Outbreak of campylobacteriosis at a senior center. J Am Geriatr Soc. 2001;49:304–7. DOIPubMedGoogle Scholar
  67. Alary  M, Nadeau  D. An outbreak of Campylobacter enteritis associated with a community water supply. Can J Public Health. 1990;81:268–71.PubMedGoogle Scholar
  68. Engberg  J, Gerner-Smidt  P, Scheutz  F, Moller  NE, On  SL, Molbak  K. Water-borne Campylobacter jejuni infection in a Danish town—a 6-week continuous source outbreak. Clin Microbiol Infect. 1998;4:648–56. DOIPubMedGoogle Scholar
  69. Godoy  P, Artigues  A, Nuin  C, Aramburu  J, Perez  M, Dominguez  A, Outbreak of gastroenteritis caused by Campylobacter jejuni transmitted through drinking water. Med Clin (Barc). 2002;119:695–8.PubMedGoogle Scholar
  70. Hanninen  ML, Haajanen  H, Pummi  T, Wermundsen  K, Katila  ML, Sarkkinen  H, Detection and typing of Campylobacter jejuni and Campylobacter coli and analysis of indicator organisms in three waterborne outbreaks in Finland. Appl Environ Microbiol. 2003;69:1391–6. DOIPubMedGoogle Scholar
  71. Jones  IG, Roworth  M. An outbreak of Escherichia coli O157 and campylobacteriosis associated with contamination of a drinking water supply. Public Health. 1996;110:277–82. DOIPubMedGoogle Scholar
  72. Holme  R. Drinking water contamination in Walkerton, Ontario: positive resolutions from a tragic event. Water Sci Technol. 2003;47:1–6.PubMedGoogle Scholar
  73. Maurer  AM, Sturchler  D. A waterborne outbreak of small round structured virus, campylobacter and shigella co-infections in La Neuveville, Switzerland, 1998. Epidemiol Infect. 2000;125:325–32. DOIPubMedGoogle Scholar
  74. Melby  K, Gondrosen  B, Gregusson  S, Ribe  H, Dahl  OP. Waterborne campylobacteriosis in northern Norway. Int J Food Microbiol. 1991;12:151–6. DOIPubMedGoogle Scholar
  75. Miettinen  IT, Zacheus  O, von Bonsdorff  CH, Vartiainen  T. Waterborne epidemics in Finland in 1998–1999. Water Sci Technol. 2001;43:67–71.PubMedGoogle Scholar
  76. Sacks  JJ, Lieb  S, Baldy  LM, Berta  S, Patton  CM, White  MC, Epidemic campylobacteriosis associated with a community water supply. Am J Public Health. 1986;76:424–8. DOIPubMedGoogle Scholar
  77. Duke  LA, Breathnach  AS, Jenkins  DR, Harkis  BA, Codd  AW. A mixed outbreak of cryptosporidium and campylobacter infection associated with a private water supply. Epidemiol Infect. 1996;116:303–8. DOIPubMedGoogle Scholar
  78. Furtado  C, Adak  GK, Stuart  JM, Wall  PG, Evans  HS, Casemore  DP. Outbreaks of waterborne infectious intestinal disease in England and Wales, 1992–5. Epidemiol Infect. 1998;121:109–19. DOIPubMedGoogle Scholar
  79. Melby  KK, Svendby  JG, Eggebo  T, Holmen  LA, Andersen  BM, Lind  L, Outbreak of Campylobacter infection in a subartic community. Eur J Clin Microbiol Infect Dis. 2000;19:542–4. DOIPubMedGoogle Scholar
  80. Rautelin  H, Koota  K, von Essen  R, Jahkola  M, Siitonen  A, Kosunen  TU. Waterborne Campylobacter jejuni epidemic in a Finnish hospital for rheumatic diseases. Scand J Infect Dis. 1990;22:321–6. DOIPubMedGoogle Scholar
  81. Stehr-Green  JK, Nicholls  C, McEwan  S, Payne  A, Mitchell  P. Waterborne outbreak of Campylobacter jejuni in Christchurch: the importance of a combined epidemiologic and microbiologic investigation. N Z Med J. 1991;104:356–8.PubMedGoogle Scholar
  82. Centers for Disease Control and Prevention. Outbreak of Escherichia coli O157:H7 and Campylobacter among attendees of the Washington County Fair—New York, 1999. MMWR Morb Mortal Wkly Rep. 1999;48:803–5.PubMedGoogle Scholar
  83. Bopp  DJ, Sauders  BD, Waring  AL, Ackelsberg  J, Dumas  N, Braun-Howland  E, Detection, isolation, and molecular subtyping of Escherichia coli O157:H7 and Campylobacter jejuni associated with a large waterborne outbreak. J Clin Microbiol. 2003;41:174–80. DOIPubMedGoogle Scholar
  84. Millson  M, Bokhout  M, Carlson  J, Spielberg  L, Aldis  R, Borczyk  A, An outbreak of Campylobacter jejuni gastroenteritis linked to meltwater contamination of a municipal well. Can J Public Health. 1991;82:27–31.PubMedGoogle Scholar
  85. Aho  M, Kurki  M, Rautelin  H, Kosunen  TU. Waterborne outbreak of Campylobacter enteritis after outdoors infantry drill in Utti, Finland. Epidemiol Infect. 1989;103:133–41. DOIPubMedGoogle Scholar
  86. Merritt  A, Miles  R, Bates  J. An outbreak of Campylobacter enteritis on an island resort, north Queensland. Commun Dis Intell. 1999;23:215–9.PubMedGoogle Scholar
  87. Said  B, Wright  F, Nichols  GL, Reacher  M, Rutter  M. Outbreaks of infectious disease associated with private drinking water supplies in England and Wales 1970–2000. Epidemiol Infect. 2003;130:469–79.PubMedGoogle Scholar
  88. Gillespie  IA, O'Brien  SJ, Frost  JA, Adak  GK, Horby  P, Swan  AV, A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg Infect Dis. 2002;8:937–42.PubMedGoogle Scholar
  89. Moore  J, Caldwell  P, Millar  B. Molecular detection of Campylobacter spp. in drinking, recreational and environmental water supplies. Int J Hyg Environ Health. 2001;204:185–9. DOIPubMedGoogle Scholar
  90. Moore  JE, Caldwell  PS, Millar  BC, Murphy  PG. Occurrence of Campylobacter spp. in water in Northern Ireland: implications for public health. Ulster Med J. 2001;70:102–7.PubMedGoogle Scholar
  91. Savill  MG, Hudson  JA, Ball  A, Klena  JD, Scholes  P, Whyte  RJ, Enumeration of Campylobacter in New Zealand recreational and drinking waters. J Appl Microbiol. 2001;91:38–46. DOIPubMedGoogle Scholar
  92. Hernandez  J, Fayos  A, Alonso  JL, Owen  RJ. Ribotypes and AP-PCR fingerprints of thermophilic campylobacters from marine recreational waters. J Appl Bacteriol. 1996;80:157–64. DOIPubMedGoogle Scholar
  93. Minaev  VI, Cherkasskii  BL, Volokhovich  TT, Minaeva  NZ, Pertin  OS, Gorelov  AV, The leading pathways and factors in the transmission of the causative agents of campylobacteriosis under current conditions. Zh Mikrobiol Epidemiol Immunobiol. 1995; (2):39–42.PubMedGoogle Scholar
  94. Goossens  H, Giesendorf  BA, Vandamme  P, Vlaes  L, Van den  BC, Koeken  A, Investigation of an outbreak of Campylobacter upsaliensis in day care centers in Brussels: analysis of relationships among isolates by phenotypic and genotypic typing methods. J Infect Dis. 1995;172:1298–305. DOIPubMedGoogle Scholar
  95. Vandamme  P, Pugina  P, Benzi  G, Van Etterijck  R, Vlaes  L, Kersters  K, Outbreak of recurrent abdominal cramps associated with Arcobacter butzleri in an Italian school. J Clin Microbiol. 1992;30:2335–7.PubMedGoogle Scholar
  96. Morooka  T, Umeda  A, Fujita  M, Matano  H, Fujimoto  S, Yukitake  K, Epidemiologic application of pulsed-field gel electrophoresis to an outbreak of Campylobacter fetus meningitis in a neonatal intensive care unit. Scand J Infect Dis. 1996;28:269–70. DOIPubMedGoogle Scholar
  97. Evans  SJ. The seasonality of canine births and human campylobacteriosis: a hypothesis. Epidemiol Infect. 1993;110:267–72. DOIPubMedGoogle Scholar
  98. Ellis  A, Irwin  R, Hockin  J, Borczyk  A, Woodward  D, Johnson  W. Outbreak of Campylobacter infection among farm workers: an occupational hazard. Can Commun Dis Rep. 1995;21:153–6.PubMedGoogle Scholar
  99. Schouls  LM, Reulen  S, Duim  B, Wagenaar  JA, Willems  RJ, Dingle  KE, Comparative genotyping of Campylobacter jejuni by amplified fragment length polymorphism, multilocus sequence typing, and short repeat sequencing: strain diversity, host range, and recombination. J Clin Microbiol. 2003;41:15–26. DOIPubMedGoogle Scholar
  100. Nielsen  EM, Engberg  J, Fussing  V, Petersen  L, Brogren  CH, On  SL. Evaluation of phenotypic and genotypic methods for subtyping Campylobacter jejuni isolates from humans, poultry, and cattle. J Clin Microbiol. 2000;38:3800–10.PubMedGoogle Scholar
  101. Savill  M, Hudson  A, Devane  M, Garrett  N, Gilpin  B, Ball  A. Elucidation of potential transmission routes of Campylobacter in New Zealand. Water Sci Technol. 2003;47:33–8.PubMedGoogle Scholar
  102. Stanley  K, Jones  K. Cattle and sheep farms as reservoirs of Campylobacter. J Appl Microbiol. 2003;94(Suppl):S104–13. DOIPubMedGoogle Scholar
  103. Jones  K, Howard  S, Wallace  JS. Intermittent shedding of thermophilic campylobacters by sheep at pasture. J Appl Microbiol. 1999;86:531–6. DOIPubMedGoogle Scholar
  104. Mann  DR, Akinbami  MA, Gould  KG, Ansari  AA. Seasonal variations in cytokine expression and cell-mediated immunity in male rhesus monkeys. Cell Immunol. 2000;200:105–15. DOIPubMedGoogle Scholar
  105. Stanley  KN, Wallace  JS, Currie  JE, Diggle  PJ, Jones  K. Seasonal variation of thermophilic campylobacters in lambs at slaughter. J Appl Microbiol. 1998;84:1111–6. DOIPubMedGoogle Scholar
  106. Stanley  KN, Wallace  JS, Currie  JE, Diggle  PJ, Jones  K. The seasonal variation of thermophilic campylobacters in beef cattle, dairy cattle and calves. J Appl Microbiol. 1998;85:472–80. DOIPubMedGoogle Scholar
  107. Willis  WL, Murray  C. Campylobacter jejuni seasonal recovery observations of retail market broilers. Poult Sci. 1997;76:314–7.PubMedGoogle Scholar
  108. Srour  SF, Rishpon  S, Rubin  L, Warman  S. An outbreak of Campylobacter jejuni enteritis after farm visit in Haifa subdistrict. Harefuah. 2002;141:683–4.PubMedGoogle Scholar
  109. Beecham  HJ III, Lebron  CI, Echeverria  P. Short report: impact of traveler's diarrhea on United States troops deployed to Thailand. Am J Trop Med Hyg. 1997;57:699–701.PubMedGoogle Scholar
  110. Mattila  L, Siitonen  A, Kyronseppa  H, Simula  I, Oksanen  P, Stenvik  M, Seasonal variation in etiology of travelers' diarrhea. Finnish-Moroccan Study Group. J Infect Dis. 1992;165:385–8. DOIPubMedGoogle Scholar
  111. Pearson  AD, Healing  TD. The surveillance and control of campylobacter infection. Commun Dis Rep CDR Rev. 1992;2:R133–9.PubMedGoogle Scholar
  112. Beecham  HJ III, Lebron  CI, Echeverria  P. Short report: impact of traveler's diarrhea on United States troops deployed to Thailand. Am J Trop Med Hyg. 1997;57:699–701.PubMedGoogle Scholar
  113. Haberberger  RL Jr, Mikhail  IA, Burans  JP, Hyams  KC, Glenn  JC, Diniega  BM, Travelers' diarrhea among United States military personnel during joint American-Egyptian armed forces exercises in Cairo, Egypt. Mil Med. 1991;156:27–30.PubMedGoogle Scholar
  114. Black  RE. Epidemiology of travelers' diarrhea and relative importance of various pathogens. Rev Infect Dis. 1990;12(Suppl 1):S73–9. DOIPubMedGoogle Scholar
  115. Black  RE. Pathogens that cause travelers' diarrhea in Latin America and Africa. Rev Infect Dis. 1986;8(Suppl 2):S131–5. DOIPubMedGoogle Scholar
  116. Brasseur  D, Casimir  G, Goyens  P. Campylobacter jejuni and infantile traveller's diarrhoea. Eur J Pediatr. 1986;144:517–8. DOIPubMedGoogle Scholar
  117. Echeverria  P, Blacklow  NR, Sanford  LB, Cukor  GG. Travelers' diarrhea among American Peace Corps volunteers in rural Thailand. J Infect Dis. 1981;143:767–71. DOIPubMedGoogle Scholar
  118. Kapperud  G, Lassen  J, Ostroff  SM, Aasen  S. Clinical features of sporadic Campylobacter infections in Norway. Scand J Infect Dis. 1992;24:741–9. DOIPubMedGoogle Scholar
  119. Pazzaglia  G, Bourgeois  AL, Araby  I, Mikhail  I, Podgore  JK, Mourad  A, Campylobacter-associated diarrhoea in Egyptian infants: epidemiology and clinical manifestations of disease and high frequency of concomitant infections. J Diarrhoeal Dis Res. 1993;11:6–13.PubMedGoogle Scholar
  120. Bichile  LS, Saraswati  K, Popat  UR, Nanivadekar  SA, Deodhar  LP. Acute Campylobacter jejuni enteritis in 385 hospitalised patients. J Assoc Physicians India. 1992;40:164–6.PubMedGoogle Scholar
  121. Louis  V, Russek-Cohen  E, Rubinstein  MI, O'Brien  SJ, Pearson  AD, Colwell  RR. Seasonality of Campylobacter cases in England and Wales (1990–1999) [abstract]. Presented at the 103rd General Meeting of the American Society for Microbiology; 2003 May 17–22; Washington, DC.

Main Article

Page created: April 25, 2012
Page updated: April 25, 2012
Page reviewed: April 25, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external