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Environ Health Perspect. 2003 Jan; 111(1): 19–28.
PMCID: PMC1241301
Research Article

Pathogen survival trajectories: an eco-environmental approach to the modeling of human campylobacteriosis ecology.


Campylobacteriosis, like many human diseases, has its own ecology in which the propagation of human infection and disease depends on pathogen survival and finding new hosts in order to replicate and sustain the pathogen population. The complexity of this process, a process common to other enteric pathogens, has hampered control efforts. Many unknowns remain, resulting in a poorly understood disease ecology. To provide structure to these unknowns and help direct further research and intervention, we propose an eco-environmental modeling approach for campylobacteriosis. This modeling approach follows the pathogen population as it moves through the environments that define the physical structure of its ecology. In this paper, we term the ecologic processes and environments through which these populations move "pathogen survival trajectories." Although such a modeling approach could have veterinary applications, our emphasis is on human campylobacteriosis and focuses on human exposures to Campylobacter through feces, food, and aquatic environments. The pathogen survival trajectories that lead to human exposure include ecologic filters that limit population size, e.g., cooking food to kill Campylobacter. Environmental factors that influence the size of the pathogen reservoirs include temperature, nutrient availability, and moisture availability during the period of time the pathogen population is moving through the environment between infected and susceptible hosts. We anticipate that the modeling approach proposed here will work symbiotically with traditional epidemiologic and microbiologic research to help guide and evaluate the acquisition of new knowledge about the ecology, eventual intervention, and control of campylobacteriosis.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Wheeler JG, Sethi D, Cowden JM, Wall PG, Rodrigues LC, Tompkins DS, Hudson MJ, Roderick PJ. Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. The Infectious Intestinal Disease Study Executive. BMJ. 1999 Apr 17;318(7190):1046–1050. [PMC free article] [PubMed]
  • Blakely TA, Woodward AJ. Ecological effects in multi-level studies. J Epidemiol Community Health. 2000 May;54(5):367–374. [PMC free article] [PubMed]
  • Harvey T, Mahaffey KR, Velazquez S, Dourson M. Holistic risk assessment: an emerging process for environmental decisions. Regul Toxicol Pharmacol. 1995 Oct;22(2):110–117. [PubMed]
  • Focks DA, Haile DG, Daniels E, Mount GA. Dynamic life table model for Aedes aegypti (Diptera: Culicidae): analysis of the literature and model development. J Med Entomol. 1993 Nov;30(6):1003–1017. [PubMed]
  • Pekkanen J, Pearce N. Environmental epidemiology: challenges and opportunities. Environ Health Perspect. 2001 Jan;109(1):1–5. [PMC free article] [PubMed]
  • Ketley JM. Pathogenesis of enteric infection by Campylobacter. Microbiology. 1997 Jan;143(Pt 1):5–21. [PubMed]
  • Hazeleger WC, Wouters JA, Rombouts FM, Abee T. Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Appl Environ Microbiol. 1998 Oct;64(10):3917–3922. [PMC free article] [PubMed]
  • José MV, Bobadilla JR. Epidemiological model of diarrhoeal diseases and its application in prevention and control. Vaccine. 1994 Feb;12(2):109–116. [PubMed]
  • Guerrant RL, Lohr JA, Williams EK. Acute infectious diarrhea. I. Epidemiology, etiology and pathogenesis. Pediatr Infect Dis. 1986 May-Jun;5(3):353–359. [PubMed]
  • Gatewood LC, Ackerman E, Ewy W, Elveback L, Fox JP. Simulation of models of enteric virus epidemics. Int J Biomed Comput. 1971 Jul;2(3):201–213. [PubMed]
  • Han AM, U KM, Hlaing T, Bozikov J, Dezelic G, Cvjetanovic B. Epidemiological model of acute bacterial and viral diarrhoeal diseases. J Diarrhoeal Dis Res. 1985 Jun;3(2):65–72. [PubMed]
  • Altekruse SF, Stern NJ, Fields PI, Swerdlow DL. Campylobacter jejuni--an emerging foodborne pathogen. Emerg Infect Dis. 1999 Jan-Feb;5(1):28–35. [PMC free article] [PubMed]
  • Oosterom J, den Uyl CH, Bänffer JR, Huisman J. Epidemiological investigations on Campylobacter jejuni in households with a primary infection. J Hyg (Lond) 1984 Oct;93(2):325–332. [PMC free article] [PubMed]
  • Harris NV, Weiss NS, Nolan CM. The role of poultry and meats in the etiology of Campylobacter jejuni/coli enteritis. Am J Public Health. 1986 Apr;76(4):407–411. [PMC free article] [PubMed]
  • Deming MS, Tauxe RV, Blake PA, Dixon SE, Fowler BS, Jones TS, Lockamy EA, Patton CM, Sikes RO. Campylobacter enteritis at a university: transmission from eating chicken and from cats. Am J Epidemiol. 1987 Sep;126(3):526–534. [PubMed]
  • Notermans S, Hoogenboom-Verdegaal A. Existing and emerging foodborne diseases. Int J Food Microbiol. 1992 Mar-Apr;15(3-4):197–205. [PubMed]
  • Eberhart-Phillips J, Walker N, Garrett N, Bell D, Sinclair D, Rainger W, Bates M. Campylobacteriosis in New Zealand: results of a case-control study. J Epidemiol Community Health. 1997 Dec;51(6):686–691. [PMC free article] [PubMed]
  • Butzler JP, Oosterom J. Campylobacter: pathogenicity and significance in foods. Int J Food Microbiol. 1991 Jan;12(1):1–8. [PubMed]
  • Pearson AD, Greenwood M, Healing TD, Rollins D, Shahamat M, Donaldson J, Colwell RR. Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl Environ Microbiol. 1993 Apr;59(4):987–996. [PMC free article] [PubMed]
  • Jones K, Betaieb M, Telford DR. Thermophilic campylobacters in surface waters around Lancaster, UK: negative correlation with Campylobacter infections in the community. J Appl Bacteriol. 1990 Nov;69(5):758–764. [PubMed]
  • Bolton FJ, Coates D, Hutchinson DN, Godfree AF. A study of thermophilic campylobacters in a river system. J Appl Bacteriol. 1987 Feb;62(2):167–176. [PubMed]
  • Mann DR, Akinbami MA, Gould KG, Ansari AA. Seasonal variations in cytokine expression and cell-mediated immunity in male rhesus monkeys. Cell Immunol. 2000 Mar 15;200(2):105–115. [PubMed]
  • Hazeleger WC, Janse JD, Koenraad PM, Beumer RR, Rombouts FM, Abee T. Temperature-dependent membrane fatty acid and cell physiology changes in coccoid forms of Campylobacter jejuni. Appl Environ Microbiol. 1995 Jul;61(7):2713–2719. [PMC free article] [PubMed]
  • Tholozan JL, Cappelier JM, Tissier JP, Delattre G, Federighi M. Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells. Appl Environ Microbiol. 1999 Mar;65(3):1110–1116. [PMC free article] [PubMed]
  • Talibart R, Denis M, Castillo A, Cappelier JM, Ermel G. Survival and recovery of viable but noncultivable forms of Campylobacter in aqueous microcosm. Int J Food Microbiol. 2000 Apr 10;55(1-3):263–267. [PubMed]
  • Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ. Experimental Campylobacter jejuni infection in humans. J Infect Dis. 1988 Mar;157(3):472–479. [PubMed]
  • Medema GJ, Teunis PF, Havelaar AH, Haas CN. Assessment of the dose-response relationship of Campylobacter jejuni. Int J Food Microbiol. 1996 Jun;30(1-2):101–111. [PubMed]
  • Morgan D, Gunneberg C, Gunnell D, Healing TD, Lamerton S, Soltanpoor N, Lewis DA, White DG. An outbreak of Campylobacter infection associated with the consumption of unpasteurised milk at a large festival in England. Eur J Epidemiol. 1994 Oct;10(5):581–585. [PubMed]
  • Riordan T, Humphrey TJ, Fowles A. A point source outbreak of campylobacter infection related to bird-pecked milk. Epidemiol Infect. 1993 Apr;110(2):261–265. [PMC free article] [PubMed]
  • Sacks JJ, Lieb S, Baldy LM, Berta S, Patton CM, White MC, Bigler WJ, Witte JJ. Epidemic campylobacteriosis associated with a community water supply. Am J Public Health. 1986 Apr;76(4):424–428. [PMC free article] [PubMed]
  • Melby K, Gondrosen B, Gregusson S, Ribe H, Dahl OP. Waterborne campylobacteriosis in northern Norway. Int J Food Microbiol. 1991 Feb;12(2-3):151–156. [PubMed]
  • Millson M, Bokhout M, Carlson J, Spielberg L, Aldis R, Borczyk A, Lior H. An outbreak of Campylobacter jejuni gastroenteritis linked to meltwater contamination of a municipal well. Can J Public Health. 1991 Jan-Feb;82(1):27–31. [PubMed]
  • Jones A, Harrop C. A study of Campylobacter enteritis. J Int Med Res. 1981;9(1):40–43. [PubMed]
  • Cawthraw SA, Lind L, Kaijser B, Newell DG. Antibodies, directed towards Campylobacter jejuni antigens, in sera from poultry abattoir workers. Clin Exp Immunol. 2000 Oct;122(1):55–60. [PMC free article] [PubMed]
  • Fernández H, Kahler K, Salazar R, Ríos MA. Prevalence of thermotolerant species of Campylobacter and their biotypes in children and domestic birds and dogs in southern Chile. Rev Inst Med Trop Sao Paulo. 1994 Sep-Oct;36(5):433–436. [PubMed]
  • Yogasundram K, Shane SM, Harrington KS. Prevalence of Campylobacter jejuni in selected domestic and wild birds in Louisiana. Avian Dis. 1989 Oct-Dec;33(4):664–667. [PubMed]
  • Blaser M, Cravens J, Powers BW, Wang WL. Campylobacter enteritis associated with canine infection. Lancet. 1978 Nov 4;2(8097):979–981. [PubMed]
  • Blaser MJ, LaForce FM, Wilson NA, Wang WL. Reservoirs for human campylobacteriosis. J Infect Dis. 1980 May;141(5):665–669. [PubMed]
  • Kapperud G, Rosef O. Avian wildlife reservoir of Campylobacter fetus subsp. jejuni, Yersinia spp., and Salmonella spp. in Norway. Appl Environ Microbiol. 1983 Feb;45(2):375–380. [PMC free article] [PubMed]
  • Luechtefeld NA, Blaser MJ, Reller LB, Wang WL. Isolation of Campylobacter fetus subsp. jejuni from migratory waterfowl. J Clin Microbiol. 1980 Sep;12(3):406–408. [PMC free article] [PubMed]
  • Ito K, Kubokura Y, Kaneko K, Totake Y, Ogawa M. Occurrence of Campylobacter jejuni in free-living wild birds from Japan. J Wildl Dis. 1988 Jul;24(3):467–470. [PubMed]
  • Maruyama S, Tanaka T, Katsube Y, Nakanishi H, Nukina M. Prevalence of thermophilic campylobacters in crows (Corvus levaillantii, Corvus corone) and serogroups of the isolates. Nihon Juigaku Zasshi. 1990 Dec;52(6):1237–1244. [PubMed]
  • Pacha RE, Clark GW, Williams EA, Carter AM. Migratory birds of central Washington as reservoirs of Campylobacter jejuni. Can J Microbiol. 1988 Jan;34(1):80–82. [PubMed]
  • Palmgren H, Sellin M, Bergström S, Olsen B. Enteropathogenic bacteria in migrating birds arriving in Sweden. Scand J Infect Dis. 1997;29(6):565–568. [PubMed]
  • Cabrita J, Rodrigues J, Bragança F, Morgado C, Pires I, Gonçalves AP. Prevalence, biotypes, plasmid profile and antimicrobial resistance of Campylobacter isolated from wild and domestic animals from northeast Portugal. J Appl Bacteriol. 1992 Oct;73(4):279–285. [PubMed]
  • Rosef O, Gondrosen B, Kapperud G, Underdal B. Isolation and characterization of Campylobacter jejuni and Campylobacter coli from domestic and wild mammals in Norway. Appl Environ Microbiol. 1983 Oct;46(4):855–859. [PMC free article] [PubMed]
  • Oosterom J, Dekker R, de Wilde GJ, van Kempen-de Troye F, Engels GB. Prevalence of Campylobacter jejuni and Salmonella during pig slaughtering. Vet Q. 1985 Jan;7(1):31–34. [PubMed]
  • Young CR, Harvey R, Anderson R, Nisbet D, Stanker LH. Enteric colonisation following natural exposure to Campylobacter in pigs. Res Vet Sci. 2000 Feb;68(1):75–78. [PubMed]
  • Weijtens MJ, Bijker PG, Van der Plas J, Urlings HA, Biesheuvel MH. Prevalence of campylobacter in pigs during fattening; an epidemiological study. Vet Q. 1993 Dec;15(4):138–143. [PubMed]
  • Weijtens MJ, van der Plas J, Bijker PG, Urlings HA, Koster D, van Logtestijn JG, Huis in't Veld JH. The transmission of campylobacter in piggeries; an epidemiological study. J Appl Microbiol. 1997 Dec;83(6):693–698. [PubMed]
  • Weijtens MJ, Reinders RD, Urlings HA, Van der Plas J. Campylobacter infections in fattening pigs; excretion pattern and genetic diversity. J Appl Microbiol. 1999 Jan;86(1):63–70. [PubMed]
  • Pearson AD, Greenwood MH, Feltham RK, Healing TD, Donaldson J, Jones DM, Colwell RR. Microbial ecology of Campylobacter jejuni in a United Kingdom chicken supply chain: intermittent common source, vertical transmission, and amplification by flock propagation. Appl Environ Microbiol. 1996 Dec;62(12):4614–4620. [PMC free article] [PubMed]
  • Jacobs-Reitsma WF, Bolder NM, Mulder RW. Cecal carriage of Campylobacter and Salmonella in Dutch broiler flocks at slaughter: a one-year study. Poult Sci. 1994 Aug;73(8):1260–1266. [PubMed]
  • Humphrey TJ, Beckett P. Campylobacter jejuni in dairy cows and raw milk. Epidemiol Infect. 1987 Jun;98(3):263–269. [PMC free article] [PubMed]
  • 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 Sep;85(3):472–480. [PubMed]
  • Wesley IV, Wells SJ, Harmon KM, Green A, Schroeder-Tucker L, Glover M, Siddique I. Fecal shedding of Campylobacter and Arcobacter spp. in dairy cattle. Appl Environ Microbiol. 2000 May;66(5):1994–2000. [PMC free article] [PubMed]
  • Meanger JD, Marshall RB. Seasonal prevalence of thermophilic Campylobacter infections in dairy cattle and a study of infection of sheep. N Z Vet J. 1989 Mar;37(1):18–20. [PubMed]
  • Jones K, Howard S, Wallace JS. Intermittent shedding of thermophilic campylobacters by sheep at pasture. J Appl Microbiol. 1999 Mar;86(3):531–536. [PubMed]
  • Stanley KN, Wallace JS, Currie JE, Diggle PJ, Jones K. Seasonal variation of thermophilic campylobacters in lambs at slaughter. J Appl Microbiol. 1998 Jun;84(6):1111–1116. [PubMed]
  • Coates D, Hutchinson DN, Bolton FJ. Survival of thermophilic campylobacters on fingertips and their elimination by washing and disinfection. Epidemiol Infect. 1987 Oct;99(2):265–274. [PMC free article] [PubMed]
  • Savill MG, Hudson JA, Ball A, Klena JD, Scholes P, Whyte RJ, McCormick RE, Jankovic D. Enumeration of Campylobacter in New Zealand recreational and drinking waters. J Appl Microbiol. 2001 Jul;91(1):38–46. [PubMed]
  • Arvanitidou M, Stathopoulos GA, Katsouyannopoulos VC. Isolation of Campylobacter and Yersinia spp. from Drinking Waters. J Travel Med. 1994 Sep 1;1(3):156–159. [PubMed]
  • Jones K, Betaieb M, Telford DR. Seasonal variation of thermophilic campylobacters in sewage sludge. J Appl Bacteriol. 1990 Aug;69(2):185–189. [PubMed]
  • Jones K, Betaieb M, Telford DR. Correlation between environmental monitoring of thermophilic campylobacters in sewage effluent and the incidence of Campylobacter infection in the community. J Appl Bacteriol. 1990 Aug;69(2):235–240. [PubMed]
  • Mawer SL. Campylobacters in man and the environment in Hull and East Yorkshire. Epidemiol Infect. 1988 Oct;101(2):287–294. [PMC free article] [PubMed]
  • Stampi S, Varoli O, de Luca G, Zanetti F. Occurrence, removal and seasonal variation of "thermophilic" campylobacters in a sewage treatment plant in Italy. Zentralbl Hyg Umweltmed. 1992 Oct;193(3):199–210. [PubMed]
  • Arvanitidou M, Stathopoulos GA, Constantinidis TC, Katsouyannopoulos V. The occurrence of Salmonella, Campylobacter and Yersinia spp. in river and lake waters. Microbiol Res. 1995 May;150(2):153–158. [PubMed]
  • Carter AM, Pacha RE, Clark GW, Williams EA. Seasonal occurrence of Campylobacter spp. in surface waters and their correlation with standard indicator bacteria. Appl Environ Microbiol. 1987 Mar;53(3):523–526. [PMC free article] [PubMed]
  • Bolton FJ, Hinchliffe PM, Coates D, Robertson L. A most probable number method for estimating small numbers of campylobacters in water. J Hyg (Lond) 1982 Oct;89(2):185–190. [PMC free article] [PubMed]
  • Stanley K, Cunningham R, Jones K. Isolation of Campylobacter jejuni from groundwater. J Appl Microbiol. 1998 Jul;85(1):187–191. [PubMed]
  • Obiri-Danso K, Jones K. Distribution and seasonality of microbial indicators and thermophilic campylobacters in two freshwater bathing sites on the River Lune in northwest England. J Appl Microbiol. 1999 Dec;87(6):822–832. [PubMed]
  • Obiri-Danso K, Jones K. The effect of a new sewage treatment plant on faecal indicator numbers, campylobacters and bathing water compliance in Morecambe Bay. J Appl Microbiol. 1999 Apr;86(4):603–614. [PubMed]
  • Obiri-Danso K, Paul N, Jones K. The effects of UVB and temperature on the survival of natural populations and pure cultures of Campylobacter jejuni, Camp. coli, Camp. lari and urease-positive thermophilic campylobacters (UPTC) in surface waters. J Appl Microbiol. 2001 Feb;90(2):256–267. [PubMed]
  • Gill CO, Harris LM. Survival and growth of Campylobacter fetus subsp. jejuni on meat and in cooked foods. Appl Environ Microbiol. 1982 Aug;44(2):259–263. [PMC free article] [PubMed]
  • Kramer JM, Frost JA, Bolton FJ, Wareing DR. Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. J Food Prot. 2000 Dec;63(12):1654–1659. [PubMed]
  • Dawkins HC, Bolton FJ, Hutchinson DN. A study of the spread of Campylobacter jejuni in four large kitchens. J Hyg (Lond) 1984 Jun;92(3):357–364. [PMC free article] [PubMed]
  • Shane SM, Montrose MS, Harrington KS. Transmission of Campylobacter jejuni by the housefly (Musca domestica). Avian Dis. 1985 Apr-Jun;29(2):384–391. [PubMed]
  • Rosef O, Kapperud G. House flies (Musca domestica) as possible vectors of Campylobacter fetus subsp. jejuni. Appl Environ Microbiol. 1983 Feb;45(2):381–383. [PMC free article] [PubMed]
  • Bolton FJ, Surman SB, Martin K, Wareing DR, Humphrey TJ. Presence of Campylobacter and Salmonella in sand from bathing beaches. Epidemiol Infect. 1999 Feb;122(1):7–13. [PMC free article] [PubMed]
  • Lázaro B, Cárcamo J, Audícana A, Perales I, Fernández-Astorga A. Viability and DNA maintenance in nonculturable spiral Campylobacter jejuni cells after long-term exposure to low temperatures. Appl Environ Microbiol. 1999 Oct;65(10):4677–4681. [PMC free article] [PubMed]
  • Hänninen ML, Hakkinen M, Rautelin H. Stability of related human and chicken Campylobacter jejuni genotypes after passage through chick intestine studied by pulsed-field gel electrophoresis. Appl Environ Microbiol. 1999 May;65(5):2272–2275. [PMC free article] [PubMed]
  • Thomas C, Hill DJ, Mabey M. Evaluation of the effect of temperature and nutrients on the survival of Campylobacter spp. in water microcosms. J Appl Microbiol. 1999 Jun;86(6):1024–1032. [PubMed]
  • Arumugaswamy RK, Proudford RW, Eyles MJ. The response of Campylobacter jejuni and Campylobacter coli in the Sydney rock oyster (Crassostrea commercialis), during depuration and storage. Int J Food Microbiol. 1988 Dec;7(3):173–183. [PubMed]
  • Jones DM, Sutcliffe EM, Curry A. Recovery of viable but non-culturable Campylobacter jejuni. J Gen Microbiol. 1991 Oct;137(10):2477–2482. [PubMed]
  • Rollins DM, Colwell RR. Viable but nonculturable stage of Campylobacter jejuni and its role in survival in the natural aquatic environment. Appl Environ Microbiol. 1986 Sep;52(3):531–538. [PMC free article] [PubMed]
  • Buswell CM, Herlihy YM, Lawrence LM, McGuiggan JT, Marsh PD, Keevil CW, Leach SA. Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl Environ Microbiol. 1998 Feb;64(2):733–741. [PMC free article] [PubMed]

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