Marked Campylobacteriosis Decline after Interventions Aimed at Poultry, New Zealand

A population-level food safety response successfully reduced disease incidence.

service (3). Campylobacteriosis notifications rose steadily after campylobacteriosis first became notifiable and peaked in 2006 at >380 per 100,000 population (4). A concomitant increase in campylobacteriosis hospitalizations has been noted, which suggests this rise in notifications is unlikely to be artifactual (5).
To help inform prevention and control strategies, research efforts have been directed at establishing the likely contributors to this rise in campylobacteriosis incidence. Consistent with international findings (6)(7)(8), New Zealand investigations implicated poultry meat as a significant source of foodborne sporadic campylobacteriosis (9)(10)(11)(12)(13). A relatively small case-control study in Christchurch in 1992-1993 reported several poultry-associated risk factors, including consumption of undercooked poultry (10). A larger national case-control study in [1994][1995] reported similar findings, with a combined population-attributable risk of poultry-related exposures >50% (9). A systematic review also concluded that poultry consumption was a prominent risk factor for sporadic campylobacteriosis in New Zealand (11). Reports noted the rise in campylobacteriosis was closely correlated with an increase in consumption of fresh poultry (14).
Microbiological source attribution approaches have also been used to estimate the contribution of different sources and transmission pathways of campylobacteriosis in New Zealand. These techniques involve examining the epidemiology of campylobacteriosis at the genotype level by comparing C. jejuni genotypes from humans with those found in a range of food and environmental sources. In 2005, a major source attribution study for campylobacteriosis was initiated at a sentinel surveillance site in the Manawatu region of New Zealand (12).
Campylobacter spp. isolates from cases notified in the region were genotyped by using multilocus sequence typing (MLST) and compared with isolates recovered from food and environmental sources (12,13). Statistical modeling was used to apportion human cases to potential disease sources, thereby estimating each source's relative importance (13,15,16). This modeling revealed that >50% of sporadic campylobacteriosis cases in the region were attributable to poultry (12,13).
On the basis of these findings, public health professionals advocated for more rigorous controls on foodborne pathways of campylobacteriosis, particularly for poultry (3,14). One intervention promoted was the freezing of all fresh poultry meat to reduce levels of Campylobacter spp. contamination, with fresh poultry allowed to be sold only when it could be shown to pose a low risk to human health (3). In late 2006, the New Zealand Food Safety Authority (NZFSA) released a risk management strategy for reducing incidence of poultryassociated foodborne campylobacteriosis.
New Zealand has a highly integrated, closed system of poultry production, with all poultry meat available for retail sale being of domestic origin. Processors of chicken meat control most aspects of production, processing, and distribution; 3 processing companies supply >90% of chicken meat consumed in New Zealand, representing 95% of all poultry meat consumed (2). As a result, interventions applied to the local poultry industry affect all domestically consumed poultry.
A marked decline in campylobacteriosis notifications was observed during 2007 and 2008 (17). We investigated this decline to assess whether it was causally related to the poultryfocused food safety interventions.

Descriptive Epidemiology
Historic notification and hospitalization data were used to calculate annual rates of campylobacteriosis In a detailed descriptive analysis, temporal trends in disease incidence and distribution were examined according to patient age, sex, socioeconomic status, ethnicity, urban versus rural dwelling, region (health board area), and season. Case-patients were assigned rurality and deprivation scores on the basis of their home domicile. For rurality assignment, we used a Statistics New Zealand classification system, which defines 7 grades of rurality on the basis of population size and employment address (18). Socioeconomic status was measured by deprivation scores assigned according to the New Zealand Deprivation Index, an area-based measure of socioeconomic position derived from the 5-year Census of Population and Dwellings (19).
The main descriptive analysis rates were calculated by using interpolated and To examine the stability of the notification system for enteric diseases during the period of interest, we compared rates for campylobacteriosis notification and hospitalization with rates for 3 other notifiable enteric diseases (salmonellosis, yersiniosis, and cryptosporidiosis). Ethical approval for this study was obtained from the Multi-Region Ethics Committee, Wellington, New Zealand.

Source Attribution
During March 2005-December 2008, C. jejuni isolates from human case-patients and environmental and food sources were collected in the Manawatu area and genotyped (sequencetyped) by using MLST (12,16). Food samples were collected from fresh meat (poultry, beef, lamb) in retail stores, and environmental water samples were collected from swimming locations in rivers. Sheep and cattle feces were sampled from farms adjacent to the catchments of these rivers.
Two models were used to apportion human cases to sources on the basis of sequence types: the modified Hald model and the Island model (12,15). The modified Hald model combines the prevalence of each C. jejuni sequence type among the sources with the observed number of human isolates of that type by using a Bayesian framework (15). This model includes source-specific and type-specific factors, and accounts for variation in the estimated prevalence.
The source-specific factor gives a measure of the ability of a source to act as a vehicle for human infection, whereas the type-specific factor yields a measure of the ability of a particular sequence type to cause disease.
The Island model uses an evolutionary model to assign sequence types to a particular source "island" or population (12). Mutation, recombination, and migration rates for isolates within and between each island are estimated by using the source isolates, and the posterior distribution of these estimates are then used to infer the origin of human isolates (12,13). To account for variations in food-processing practices that may affect the likelihood of human infection from each food source, we further extended both models to examine whether changes had occurred over time in the relative contribution of different sources to human campylobacteriosis (dynamic modeling) (21).

Key Informant Interviews and Policy Review
Key informants (n = 12), including industry and food safety experts, were interviewed to obtain information on interventions implemented to reduce Campylobacter spp. contamination in poultry. We used information from these interviews together with a review of policy documents from NZFSA and the poultry industry to formulate a summary of the interventions implemented from 2006 through 2008.

Descriptive Epidemiology
The time-trend analysis of annual notification and hospitalization rates demonstrates a steady rise and then a marked decline in the incidence of campylobacteriosis ( Figure 1

Summary of Interventions
Specific food safety and poultry industry interventions were implemented beginning in 2006, in line with NZFSA's strategy for reducing the incidence of foodborne campylobacteriosis (Table). From April 2007, poultry processors monitored and reported to the NZFSAadministered National Microbiological Database Campylobacter spp. prevalence in poultry flocks by using presence/absence cecal testing and Campylobacter spp. contamination levels in poultry carcass rinsates at the end of primary processing (Table).
In April 2008, mandatory Campylobacter spp. performance targets were introduced based on enumerated levels of Campylobacter spp. contamination on poultry carcasses at the end of primary processing, with escalating regulatory responses if targets were not met (22). NZFSA has subsequently released an updated Campylobacter Risk Management Strategy (23).
Key informants noted that attention to detail with hygienic practices throughout production and primary processing and alterations to the immersion-chiller conditions were key areas in which improvements were made. Furthermore, the monitoring of Campylobacter spp. contamination levels in poultry carcass rinsates at the end of primary processing and setting mandatory Campylobacter spp. performance targets (rather than mandating specific interventions) were viewed by both industry and regulator informants as key facilitators of the strategy's success. Although substantial evidence exists that poultry industry interventions contributed to the decline in campylobacteriosis incidence in New Zealand, several alternative explanations should be considered. These include the possibility of surveillance artifact, declining poultry consumption, declining disease associated with other foods or drinking water, effects of climate, and changes in consumer behavior.

Discussion
Surveillance artifact is unlikely to have contributed significantly to the decline, however, given the magnitude of the reduction, the similarity of temporal trends in hospitalization and notification data (Figure 1), the decline occurring across all population subgroups, and the lack of similar declines for the comparison group of notifiable enteric diseases (Figure 3). However, the lack of decline in salmonellosis is not surprising in the New Zealand context because Salmonella spp. contamination levels were very low in poultry before the implementation of these interventions (29).
To assess the possible impact of poultry consumption on the decline in campylobacteriosis, we examined poultry production data. In New Zealand, poultry production approximates poultry consumption because of the closed nature of the production system. Over the period of the marked decline in campylobacteriosis incidence (2006)(2007)(2008), fresh poultry production waned by only 5.8% (30). While this fall in production could have affected the incidence of poultry-associated foodborne campylobacteriosis, it is unlikely to be sufficient to explain the >50% drop in campylobacteriosis notifications occurring over this period.
Several foodborne pathways of campylobacteriosis (other than poultry) have been identified, including red meat and raw milk consumption (8,31). The contribution of these pathways to sporadic campylobacteriosis in New Zealand has been estimated to be notably less than that of poultry (9,12). The magnitude of the decrease seen in 2008 is such that even if the contributions from food sources other than poultry had been eliminated in their entirety, they likely could not account for the observed decline in campylobacteriosis.
Contaminated water and other environmental sources have been implicated as a transmission pathway of human campylobacteriosis (32,33). Although water is found to be contaminated with Campylobacter spp., molecular epidemiologic studies have shown a low similarity between these genotypes and those found in human case-patients, suggesting that the strains detected in water are relatively apathogenic or that humans have limited exposure to them (12,13). Furthermore, a high proportion of New Zealanders receive treated community water supplies, with only small gradual increases in the proportion receiving water that meets microbiological quality criteria (34).
Changes in consumer behavior (e.g., hygiene, food preparation, eating out) could have plausibly contributed to the decline. However, challenges in altering consumer behavior have been acknowledged (35), and, given the rapidity of the decline in incidence, it is unlikely a sudden, marked change in consumer behavior could have been a key driver of the decline.
The effect of climate was considered as a possible driver of the decline. Despite the seasonal pattern observed for campylobacteriosis, the main drivers of the association between climate and campylobacteriosis remain elusive (36). However, the rapidity of the fall in incidence suggests that global climate change factors are unlikely to be key drivers.
A strength of this study is the multiple data sources that were accessed and analyzed, including source attribution techniques and key informant interviews. Nevertheless, a limitation of this study in determining the likely cause of the recent decline in campylobacteriosis is the descriptive nature of the epidemiologic analysis and the complex epidemiology of campylobacteriosis, which means that not all factors that might influence the disease's incidence were examined explicitly. Although validated by studies in 2 other regions, the source attribution analyses were from 1 sentinel site only, and this work also has its own limitations (12,13,15). A further weakness is that details of specific industry-level interventions to reduce poultry contamination are not in the public domain, and therefore cannot be examined in detail. We were also unable to examine in detail data on Campylobacter spp. contamination levels of poultry. Rates of campylobacteriosis have shown marked annual variations in the past, so it will be important to assess medium-to long-term trends in disease and its attribution to assess the effects of NZFSA's strategy. Notification and hospitalization data for 2009 indicate that the decline in incidence seen in 2008 has been largely sustained (Figure 1). Despite the 2009 rates being slightly higher than those of 2008, they still represent a substantial decline compared with the average for 2002-2006 (48% for notifications and 50% for hospitalizations).
Although there are costs associated with implementing industry regulation, these are likely to be offset by both the direct and indirect savings from reduced disease effects and lost productivity, conservatively estimated to have cost NZ$600 per campylobacteriosis case in 2005 (37). Given an estimated 70,000 fewer cases of campylobacteriosis in the community in 2008 than in 2006, this decline represents notable savings to New Zealand society. While progress has been made in responding to New Zealand's campylobacteriosis epidemic, the costs and effects are still significant. As such, further research (including evaluating additional interventions) is desirable from a public health perspective to enable continued reductions of the still high burden posed by campylobacteriosis.
The findings of this study provide evidence of a successful population-level food safety response to a serious public health issue. New Zealand has experienced a prolonged national epidemic of campylobacteriosis. Fresh poultry, of which consumption was rising, was implicated as the dominant source, and a range of voluntary and regulatory interventions were introduced to reduce Campylobacter contamination of poultry. The apparent success of these interventions demonstrates approaches other countries could consider for controlling infectious disease epidemics linked to specific food sources. This example highlights the importance of integrated public health surveillance that includes upstream hazards as well as disease (38). Finally, the success of the response shows the value of collaboration between industry, food safety regulators, and public health researchers in addressing important food safety issues.