Molecular and spatial epidemiology of human campylobacteriosis: source association and genotype-related risk factors

SUMMARY The epidemiology of human campylobacteriosis is complex but in recent years understanding of this disease has advanced considerably. Despite being a major public health concern in many countries, the presence of multiple hosts, genotypes and transmission pathways has made it difficult to identify and quantify the determinants of human infection and disease. This has delayed the development of successful intervention programmes for this disease in many countries including New Zealand, a country with a comparatively high, yet until recently poorly understood, rate of notified disease. This study investigated the epidemiology of Campylobacter jejuni at the genotype-level over a 3-year period between 2005 and 2008 using multilocus sequence typing. By combining epidemiological surveillance and population genetics, a dominant, internationally rare strain of C. jejuni (ST474) was identified, and most human cases (65·7%) were found to be caused by only seven different genotypes. Source association of genotypes was used to identify risk factors at the genotype-level through multivariable logistic regression and a spatial model. Poultry-associated cases were more likely to be found in urban areas compared to rural areas. In particular young children in rural areas had a higher risk of infection with ruminant strains than their urban counterparts. These findings provide important information for the implementation of pathway-specific control strategies.

[1]  P. Scholes,et al.  The Transmission of Thermotolerant Campylobacter spp. to People Living or Working on Dairy Farms in New Zealand , 2008, Zoonoses and public health.

[2]  S. O'Brien,et al.  Milkborne general outbreaks of infectious intestinal disease, England and Wales, 1992–2000 , 2003, Epidemiology and Infection.

[3]  P. Scholes,et al.  The occurrence of Campylobacter subtypes in environmental reservoirs and potential transmission routes , 2005, Journal of applied microbiology.

[4]  J. Cheesbrough,et al.  Specific detection of Campylobacter jejuni from faeces using single nucleotide polymorphisms , 2006, Epidemiology and Infection.

[5]  N. Wilson,et al.  Regulation of chicken contamination is urgently needed to control New Zealand's serious campylobacteriosis epidemic. , 2006, The New Zealand medical journal.

[6]  M. Murray,et al.  Determinants of cluster distribution in the molecular epidemiology of tuberculosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Garrett,et al.  Estimated number of cases of foodborne infectious disease in New Zealand. , 2000, The New Zealand medical journal.

[8]  M. Maiden,et al.  Multi-locus sequence typing: a tool for global epidemiology. , 2003, Trends in microbiology.

[9]  F. Mégraud,et al.  The seasonal distribution of campylobacter infection in nine European countries and New Zealand , 2002, Epidemiology and Infection.

[10]  Eduardo N. Taboada,et al.  Epidemiology, Relative Invasive Ability, Molecular Characterization, and Competitive Performance of Campylobacter jejuni Strains in the Chicken Gut , 2007, Applied and Environmental Microbiology.

[11]  Gehua Wang,et al.  Use of the Oxford Multilocus Sequence Typing Protocol and Sequencing of the Flagellin Short Variable Region To Characterize Isolates from a Large Outbreak of Waterborne Campylobacter sp. Strains in Walkerton, Ontario, Canada , 2005, Journal of Clinical Microbiology.

[12]  Daniel J. Wilson,et al.  Tracing the Source of Campylobacteriosis , 2008, PLoS genetics.

[13]  J. Besag,et al.  Bayesian image restoration, with two applications in spatial statistics , 1991 .

[14]  M. Kirk,et al.  Population-Attributable Risk Estimates for Risk Factors Associated with Campylobacter Infection, Australia , 2008, Emerging infectious diseases.

[15]  J. Crump,et al.  Emerging infectious diseases in an island ecosystem: the New Zealand perspective. , 2001, Emerging infectious diseases.

[16]  J. Dallas,et al.  Campylobacter Immunity and Coinfection following a Large Outbreak in a Farming Community , 2008, Journal of Clinical Microbiology.

[17]  J. Klena,et al.  Enumeration of Campylobacter in New Zealand recreational and drinking waters , 2001, Journal of applied microbiology.

[18]  Q. Syed,et al.  Campylobacter jejuni Multilocus Sequence Types in Humans, Northwest England, 2003–2004 , 2006, Emerging infectious diseases.

[19]  P. Scholes,et al.  Survival of Campylobacter spp. in bovine faeces on pasture , 2009, Letters in applied microbiology.

[20]  Natalie D. Chrystal,et al.  Counts of Campylobacter spp. and prevalence of Salmonella associated with New Zealand broiler carcasses. , 2008, Journal of food protection.

[21]  D. Falush,et al.  Sequence Typing and Comparison of Population Biology of Campylobacter coli and Campylobacter jejuni , 2005, Journal of Clinical Microbiology.

[22]  B. Holland,et al.  Molecular Epidemiology of Campylobacter jejuni Isolates from Wild-Bird Fecal Material in Children's Playgrounds , 2008, Applied and Environmental Microbiology.

[23]  R. Davies,et al.  Survey of the prevalence of Salmonella on commercial broiler farms in the United Kingdom, 2005/06 , 2008, Veterinary Record.

[24]  Simon E F Spencer,et al.  Source Attribution of Food‐Borne Zoonoses in New Zealand: A Modified Hald Model , 2009, Risk analysis : an official publication of the Society for Risk Analysis.

[25]  S. Sheppard,et al.  Attribution of Campylobacter infections in northeast Scotland to specific sources by use of multilocus sequence typing. , 2009, The Journal of infectious diseases.

[26]  C. Nicol,et al.  Prevalence, numbers, and subtypes of Campylobacter jejuni and Campylobacter coli in uncooked retail meat samples. , 2007, Journal of food protection.

[27]  N. French,et al.  Wide geographical distribution of internationally rare Campylobacter clones within New Zealand , 2007, Epidemiology and Infection.

[28]  D. Tompkins,et al.  Demographic determinants for Campylobacter infection in England and Wales: implications for future epidemiological studies , 2008, Epidemiology and Infection.

[29]  R. Juste,et al.  Prevalence and strain diversity of thermophilic campylobacters in cattle, sheep and swine farms , 2007, Journal of applied microbiology.

[30]  J. Dallas,et al.  Has Retail Chicken Played a Role in the Decline of Human Campylobacteriosis? , 2007, Applied and Environmental Microbiology.

[31]  P. Horby,et al.  A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. , 2002, Emerging infectious diseases.

[32]  Daniel Falush,et al.  Campylobacter genotyping to determine the source of human infection. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[33]  M. Baker,et al.  Is the major increase in notified campylobacteriosis in New Zealand real? , 2006, Epidemiology and Infection.

[34]  S. O'Brien,et al.  Public health implications of campylobacter outbreaks in England and Wales, 1995–9: epidemiological and microbiological investigations , 2002, Epidemiology and Infection.

[35]  Daniel J. Wilson,et al.  Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. , 2009, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[36]  Q. Syed,et al.  Identification of Potential Environmentally Adapted Campylobacter jejuni Strain, United Kingdom , 2008, Emerging infectious diseases.

[37]  P. Weinstein,et al.  The regionality of campylobacteriosis seasonality in New Zealand , 2003, International journal of environmental health research.

[38]  Eduardo N. Taboada,et al.  Comparative genomic assessment of Multi-Locus Sequence Typing: rapid accumulation of genomic heterogeneity among clonal isolates of Campylobacter jejuni , 2008, BMC Evolutionary Biology.

[39]  W. van Pelt,et al.  Immunity to Campylobacter: its role in risk assessment and epidemiology , 2009, Critical reviews in microbiology.