Journal Articles
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Item Campylobacter colonization and undernutrition in infants in rural eastern Ethiopia - a longitudinal community-based birth cohort study.(Frontiers Media S.A., 2025-01-07) Chen D; McKune SL; Yang Y; Usmane IA; Ahmed IA; Amin JK; Ibrahim AM; Seran AJ; Shaik N; Ojeda A; Hassen BM; Deblais L; Ahmedo BU; Hassen KA; Bhrane M; Li X; Singh N; Roba KT; French NP; Rajashekara G; Manary MJ; Hassen JY; Havelaar AH; CAGED Research TeamBackground: Campylobacter is associated with environmental enteric dysfunction (EED) and malnutrition in children. Campylobacter infection could be a linchpin between livestock fecal exposure and health outcomes in low-resource smallholder settings. Methods: We followed a birth cohort of 106 infants in rural smallholder households in eastern Ethiopia up to 13 months of age. We measured anthropometry, surveyed sociodemographic determinants, and collected stool and urine samples. A short survey was conducted during monthly visits, infant stool samples were collected, and Campylobacter spp. was quantified using genus-specific qPCR. In month 13, we collected stool and urine samples to assay for EED biomarkers. We employed regression analyses to assess the associations of household determinants with Campylobacter colonization, EED, and growth faltering. Results: The Campylobacter load in infant stools increased with age. The mean length-for-age Z-score (LAZ) decreased from −0.45 at 3–4 months of age to −2.06 at 13 months, while the prevalence of stunting increased from 3 to 51%. The prevalence of EED at 13 months of age was 56%. A higher Campylobacter load was associated with more frequent diarrhea. Prelacteal feeding significantly increased Campylobacter load in the first month of life. Over the whole follow-up period, Campylobacter load was increased by keeping chickens unconfined at home and unsanitary disposal of infant stools while decreased by mothers’ handwashing with soap. Longitudinally, Campylobacter load was positively associated with food insecurity, introduction of complementary foods, and raw milk consumption. There were no significant associations between Campylobacter load, EED, and LAZ. Conclusion: This study found that most determinants associated with increased Campylobacter infection were related to suboptimal feeding practices and hygiene. The findings related to livestock-associated risks were inconclusive. Although stunting, EED, and Campylobacter prevalence rates all increased to high levels by the end of the first year of life, no significant association between them was identified. While additional research is needed to investigate whether findings from this study are replicable in other populations, community efforts to improve infant and young child feeding practices and food hygiene, and water, sanitation, and hygiene (WaSH) at the household level, could reduce (cross-)contamination at the point of exposure.Item New Campylobacter Lineages in New Zealand Freshwater: Pathogenesis and Public Health Implications(John Wiley and Sons, 2024-12) Cookson AL; Burgess S; Midwinter AC; Marshall JC; Moinet M; Rogers L; Fayaz A; Biggs PJ; Brightwell GThis study investigated the diversity of thermophilic Campylobacter species isolated from three New Zealand freshwater catchments affected by pastoral and urban activities. Utilising matrix-assisted laser desorption ionisation-time of flight and whole genome sequence analysis, the study identified Campylobacter jejuni (n = 46, 46.0%), C. coli (n = 39, 39%), C. lari (n = 4, 4.0%), and two novel Campylobacter species lineages (n = 11, 11%). Core genome sequence analysis provided evidence of prolonged persistence or continuous faecal shedding of closely related strains. The C. jejuni isolates displayed distinct sequence types (STs) associated with human, ruminant, and environmental sources, whereas the C. coli STs included waterborne ST3302 and ST7774. Recombination events affecting loci implicated in human pathogenesis and environmental persistence were observed, particularly in the cdtABC operon (encoding the cytolethal distending toxin) of non-human C. jejuni STs. A low diversity of antimicrobial resistance genes (aadE-Cc in C. coli), with genotype/phenotype concordance for tetracycline resistance (tetO) in three ST177 isolates, was noted. The data suggest the existence of two types of naturalised waterborne Campylobacter: environmentally persistent strains originating from waterbirds and new environmental species not linked to human campylobacteriosis. Identifying and understanding naturalised Campylobacter species is crucial for accurate waterborne public health risk assessments and the effective allocation of resources for water quality management.Item Genomic diversity of Campylobacter jejuni and Campylobacter coli isolates recovered from human and poultry in Australia and New Zealand, 2017 to 2019.(Microbiology Society, 2024-11-05) Cribb DM; Biggs PJ; McLure AT; Wallace RL; French NP; Glass K; Kirk MDWe used genomic and epidemiological data to assess and compare the population structure and origins of Campylobacter, a major foodborne pathogen, in two neighbouring countries with strong trade and cultural links, similar poultry production systems and frequent movement of people and food products. The most common sequence types (STs) differed between Australia and New Zealand, with many unique to each country. Over half of all STs were represented by a single isolate. Multidrug-resistant (MDR) genotypes were detected in 0.8% of all samples, with no MDR isolates detected in poultry. Quinolone and tetracycline resistant ST6964 was prevalent in New Zealand (10.6% of C. jejuni). Closely related isolates suggested some similar food sources or contacts. We have shown that there is little genetic overlap in human and poultry STs of Campylobacter between the countries, which highlights that this common foodborne pathogen has domestic origins in Australia and New Zealand.Item Population Structure and Antimicrobial Resistance in Campylobacter jejuni and C. coli Isolated from Humans with Diarrhea and from Poultry, East Africa.(Centers for Disease Control and Prevention, 2024-10) French NP; Thomas KM; Amani NB; Benschop J; Bigogo GM; Cleaveland S; Fayaz A; Hugho EA; Karimuribo ED; Kasagama E; Maganga R; Melubo ML; Midwinter AC; Mmbaga BT; Mosha VV; Mshana FI; Munyua P; Ochieng JB; Rogers L; Sindiyo E; Swai ES; Verani JR; Widdowson M-A; Wilkinson DA; Kazwala RR; Crump JA; Zadoks RNCampylobacteriosis and antimicrobial resistance (AMR) are global public health concerns. Africa is estimated to have the world's highest incidence of campylobacteriosis and a relatively high prevalence of AMR in Campylobacter spp. from humans and animals. Few studies have compared Campylobacter spp. isolated from humans and poultry in Africa using whole-genome sequencing and antimicrobial susceptibility testing. We explored the population structure and AMR of 178 Campylobacter isolates from East Africa, 81 from patients with diarrhea in Kenya and 97 from 56 poultry samples in Tanzania, collected during 2006-2017. Sequence type diversity was high in both poultry and human isolates, with some sequence types in common. The estimated prevalence of multidrug resistance, defined as resistance to >3 antimicrobial classes, was higher in poultry isolates (40.9%, 95% credible interval 23.6%-59.4%) than in human isolates (2.5%, 95% credible interval 0.3%-6.8%), underlining the importance of antimicrobial stewardship in livestock systems.Item Source attribution of campylobacteriosis in Australia, 2017-2019.(John Wiley and Sons, Inc., 2023-12-01) McLure A; Smith JJ; Firestone SM; Kirk MD; French N; Fearnley E; Wallace R; Valcanis M; Bulach D; Moffatt CRM; Selvey LA; Jennison A; Cribb DM; Glass KCampylobacter jejuni and Campylobacter coli infections are the leading cause of foodborne gastroenteritis in high-income countries. Campylobacter colonizes a variety of warm-blooded hosts that are reservoirs for human campylobacteriosis. The proportions of Australian cases attributable to different animal reservoirs are unknown but can be estimated by comparing the frequency of different sequence types in cases and reservoirs. Campylobacter isolates were obtained from notified human cases and raw meat and offal from the major livestock in Australia between 2017 and 2019. Isolates were typed using multi-locus sequence genotyping. We used Bayesian source attribution models including the asymmetric island model, the modified Hald model, and their generalizations. Some models included an "unsampled" source to estimate the proportion of cases attributable to wild, feral, or domestic animal reservoirs not sampled in our study. Model fits were compared using the Watanabe-Akaike information criterion. We included 612 food and 710 human case isolates. The best fitting models attributed >80% of Campylobacter cases to chickens, with a greater proportion of C. coli (>84%) than C. jejuni (>77%). The best fitting model that included an unsampled source attributed 14% (95% credible interval [CrI]: 0.3%-32%) to the unsampled source and only 2% to ruminants (95% CrI: 0.3%-12%) and 2% to pigs (95% CrI: 0.2%-11%) The best fitting model that did not include an unsampled source attributed 12% to ruminants (95% CrI: 1.3%-33%) and 6% to pigs (95% CrI: 1.1%-19%). Chickens were the leading source of human Campylobacter infections in Australia in 2017-2019 and should remain the focus of interventions to reduce burden.Item Genomic and clinical characteristics of campylobacteriosis in Australia.(Microbiology Society, 2024-01) Cribb DM; Moffatt CRM; Wallace RL; McLure AT; Bulach D; Jennison AV; French N; Valcanis M; Glass K; Kirk MDCampylobacter spp. are a common cause of bacterial gastroenteritis in Australia, primarily acquired from contaminated meat. We investigated the relationship between genomic virulence characteristics and the severity of campylobacteriosis, hospitalisation, and other host factors.We recruited 571 campylobacteriosis cases from three Australian states and territories (2018-2019). We collected demographic, health status, risk factors, and self-reported disease data. We whole genome sequenced 422 C. jejuni and 84 C. coli case isolates along with 616 retail meat isolates. We classified case illness severity using a modified Vesikari scoring system, performed phylogenomic analysis, and explored risk factors for hospitalisation and illness severity.On average, cases experienced a 7.5 day diarrhoeal illness with additional symptoms including stomach cramps (87.1 %), fever (75.6 %), and nausea (72.0 %). Cases aged ≥75 years had milder symptoms, lower Vesikari scores, and higher odds of hospitalisation compared to younger cases. Chronic gastrointestinal illnesses also increased odds of hospitalisation. We observed significant diversity among isolates, with 65 C. jejuni and 21 C. coli sequence types. Antimicrobial resistance genes were detected in 20.4 % of isolates, but multidrug resistance was rare (0.04 %). Key virulence genes such as cdtABC (C. jejuni) and cadF were prevalent (>90 % presence) but did not correlate with disease severity or hospitalisation. However, certain genes (e.g. fliK, Cj1136, and Cj1138) appeared to distinguish human C. jejuni cases from food source isolates.Campylobacteriosis generally presents similarly across cases, though some are more severe. Genotypic virulence factors identified in the literature to-date do not predict disease severity but may differentiate human C. jejuni cases from food source isolates. Host factors like age and comorbidities have a greater influence on health outcomes than virulence factors.Item A mathematical, classical stratification modeling approach to disentangling the impact of weather on infectious diseases: A case study using spatio-temporally disaggregated Campylobacter surveillance data for England and Wales.(Public Library of Science (PLoS), 2024-01-18) Lo Iacono G; Cook AJC; Derks G; Fleming LE; French N; Gillingham EL; Gonzalez Villeta LC; Heaviside C; La Ragione RM; Leonardi G; Sarran CE; Vardoulakis S; Senyah F; van Vliet AHM; Nichols G; Vega NDisentangling the impact of the weather on transmission of infectious diseases is crucial for health protection, preparedness and prevention. Because weather factors are co-incidental and partly correlated, we have used geography to separate out the impact of individual weather parameters on other seasonal variables using campylobacteriosis as a case study. Campylobacter infections are found worldwide and are the most common bacterial food-borne disease in developed countries, where they exhibit consistent but country specific seasonality. We developed a novel conditional incidence method, based on classical stratification, exploiting the long term, high-resolution, linkage of approximately one-million campylobacteriosis cases over 20 years in England and Wales with local meteorological datasets from diagnostic laboratory locations. The predicted incidence of campylobacteriosis increased by 1 case per million people for every 5° (Celsius) increase in temperature within the range of 8°-15°. Limited association was observed outside that range. There were strong associations with day-length. Cases tended to increase with relative humidity in the region of 75-80%, while the associations with rainfall and wind-speed were weaker. The approach is able to examine multiple factors and model how complex trends arise, e.g. the consistent steep increase in campylobacteriosis in England and Wales in May-June and its spatial variability. This transparent and straightforward approach leads to accurate predictions without relying on regression models and/or postulating specific parameterisations. A key output of the analysis is a thoroughly phenomenological description of the incidence of the disease conditional on specific local weather factors. The study can be crucially important to infer the elusive mechanism of transmission of campylobacteriosis; for instance, by simulating the conditional incidence for a postulated mechanism and compare it with the phenomenological patterns as benchmark. The findings challenge the assumption, commonly made in statistical models, that the transformed mean rate of infection for diseases like campylobacteriosis is a mere additive and combination of the environmental variables.Item Prevalence and Load of the Campylobacter Genus in Infants and Associated Household Contacts in Rural Eastern Ethiopia: a Longitudinal Study from the Campylobacter Genomics and Environmental Enteric Dysfunction (CAGED) Project(American Society for Microbiology, 2023-07-26) Deblais L; Ojeda A; Brhane M; Mummed B; Hassen KA; Ahmedo BU; Weldesenbet YD; Amin JK; Ahmed IA; Usmane IA; Yusuf EA; Seran AJ; Abrahim FI; Game HT; Mummed BA; Usmail MM; Umer KA; Dawid MM; Gebreyes W; French N; Hassen JY; Roba KT; Mohammed A; Yimer G; Saleem C; Chen D; Singh N; Manary MJ; McKune SL; Havelaar AH; Rajashekara G; Elkins CAIn our previous cross-sectional study, multiple species of Campylobacter were detected (88%) in stool samples from children (12 to 14 months of age) in rural eastern Ethiopia. This study assessed the temporal fecal carriage of Campylobacter in infants and identified putative reservoirs associated with these infections in infants from the same region. The prevalence and load of Campylobacter were determined using genus-specific real-time PCR. Stool samples from 106 infants (n = 1,073) were collected monthly from birth until 376 days of age (DOA). Human stool samples (mothers and siblings), livestock feces (cattle, chickens, goats, and sheep), and environmental samples (soil and drinking water) from the 106 households were collected twice per household (n = 1,644). Campylobacter was most prevalent in livestock feces (goats, 99%; sheep, 98%; cattle, 99%; chickens, 93%), followed by human stool samples (siblings, 91%; mothers, 83%; infants, 64%) and environmental samples (soil, 58%; drinking water, 43%). The prevalence of Campylobacter in infant stool samples significantly increased with age, from 30% at 27 DOA to 89% at 360 DOA (1% increase/day in the odds of being colonized) (P < 0.001). The Campylobacter load increased linearly (P < 0.001) with age from 2.95 logs at 25 DOA to 4.13 logs at 360 DOA. Within a household, the Campylobacter load in infant stool samples was positively correlated with the load in mother stool samples (r2 = 0.18) and soil collected inside the house (r2 = 0.36), which were in turn both correlated with Campylobacter loads in chicken and cattle feces (0.60 < r2 < 0.63) (P < 0.01). In conclusion, a high proportion of infants are infected with Campylobacter in eastern Ethiopia, and contact with the mother and contaminated soil may be associated with early infections. IMPORTANCE A high Campylobacter prevalence during early childhood has been associated with environmental enteric dysfunction (EED) and stunting, especially in low-resource settings. Our previous study demonstrated that Campylobacter was frequently found (88%) in children from eastern Ethiopia; however, little is known about potential Campylobacter reservoirs and transmission pathways leading to infection of infants by Campylobacter during early growth. In the longitudinal study presented here, Campylobacter was frequently detected in infants within the 106 surveyed households from eastern Ethiopia, and the prevalence was age dependent. Furthermore, preliminary analyses highlighted the potential role of the mother, soil, and livestock in the transmission of Campylobacter to the infant. Further work will explore the species and genetic composition of Campylobacter in infants and putative reservoirs using PCR and whole-genome and metagenomic sequencing. The findings from these studies can lead to the development of interventions to minimize the risk of transmission of Campylobacter to infants and, potentially, EED and stunting.Item The impact of primary and secondary processing steps on Campylobacter concentrations on chicken carcasses and portions(Elsevier Ltd, 2023-04) Kingsbury JM; Horn B; Armstrong B; Midwinter A; Biggs P; Callander M; Mulqueen K; Brooks M; van der Logt P; Biggs RCampylobacteriosis is the most commonly notified foodborne disease in New Zealand and poultry meat is the major source for human infection. Carcasses and portions were sampled from key points along primary and secondary processing chains of three New Zealand poultry processors to determine the impact of processing steps on Campylobacter concentrations. Primary processing reduced Campylobacter concentrations on carcasses by almost 6-log; the biggest reduction was achieved by the spinchill, followed by the scald step. Significant plant differences in the degree of Campylobacter reduction were also observed at these steps. The spinchill and final acidified sodium chlorite wash resulted in carcasses with low-to-no levels of Campylobacter regardless of concentrations at prior steps. A similar study was conducted at primary processing for one plant in 2013; significant improvements in Campylobacter mitigation since 2013 were noted. Campylobacter concentrations from final product from secondary processing were higher than concentrations at the end of primary processing. Drumsticks had lower Campylobacter concentrations than other portion types. Skin removal from product did not consistently result in product with lower Campylobacter concentrations. Results identify key areas to target for further reduction of Campylobacter on poultry meat, and provide a benchmark to compare the efficacy of future interventions.Item Risk factors for campylobacteriosis in Australia: outcomes of a 2018-2019 case-control study(BioMed Central Ltd, 2022-12) Cribb DM; Varrone L; Wallace RL; McLure AT; Smith JJ; Stafford RJ; Bulach DM; Selvey LA; Firestone SM; French NP; Valcanis M; Fearnley EJ; Sloan-Gardner TS; Graham T; Glass K; Kirk MDBACKGROUND: We aimed to identify risk factors for sporadic campylobacteriosis in Australia, and to compare these for Campylobacter jejuni and Campylobacter coli infections. METHODS: In a multi-jurisdictional case-control study, we recruited culture-confirmed cases of campylobacteriosis reported to state and territory health departments from February 2018 through October 2019. We recruited controls from notified influenza cases in the previous 12 months that were frequency matched to cases by age group, sex, and location. Campylobacter isolates were confirmed to species level by public health laboratories using molecular methods. We conducted backward stepwise multivariable logistic regression to identify significant risk factors. RESULTS: We recruited 571 cases of campylobacteriosis (422 C. jejuni and 84 C. coli) and 586 controls. Important risk factors for campylobacteriosis included eating undercooked chicken (adjusted odds ratio [aOR] 70, 95% CI 13-1296) or cooked chicken (aOR 1.7, 95% CI 1.1-2.8), owning a pet dog aged < 6 months (aOR 6.4, 95% CI 3.4-12), and the regular use of proton-pump inhibitors in the 4 weeks prior to illness (aOR 2.8, 95% CI 1.9-4.3). Risk factors remained similar when analysed specifically for C. jejuni infection. Unique risks for C. coli infection included eating chicken pâté (aOR 6.1, 95% CI 1.5-25) and delicatessen meats (aOR 1.8, 95% CI 1.0-3.3). Eating any chicken carried a high population attributable fraction for campylobacteriosis of 42% (95% CI 13-68), while the attributable fraction for proton-pump inhibitors was 13% (95% CI 8.3-18) and owning a pet dog aged < 6 months was 9.6% (95% CI 6.5-13). The population attributable fractions for these variables were similar when analysed by campylobacter species. Eating delicatessen meats was attributed to 31% (95% CI 0.0-54) of cases for C. coli and eating chicken pâté was attributed to 6.0% (95% CI 0.0-11). CONCLUSIONS: The main risk factor for campylobacteriosis in Australia is consumption of chicken meat. However, contact with young pet dogs may also be an important source of infection. Proton-pump inhibitors are likely to increase vulnerability to infection.