Use of Fly Screens to Reduce Campylobacter spp. Introduction in Broiler Houses

Fly screens that prevented influx of flies in 20 broiler houses during the summer of 2006 in Denmark caused a decrease in Campylobacter spp.–positive flocks from 51.4% in control houses to 15.4% in case houses. A proportional reduction in the incidence of chicken-borne campylobacteriosis can be expected by comprehensive intervention against flies in broiler production houses.

C ampylobacteriosis is a severe gastroenteric human disease of global signifi cance. The incidence correlates with the prevalence of thermophilic Campylobacter spp., predominantly C. jejuni and C. coli (1), in chickens and follows a seasonal cycle in temperate climates for reasons not fully elucidated. The number of cases is lowest in winter and highest in summer (2). In Denmark, the prevalence of Campylobacter spp.-infected chicken fl ocks peaked at 60%-80% in recent summers (3). The population size of fl ies displays a similar cycle (4). Flies, in particular the house fl y, Musca domestica, are well-known vectors of several enteric bacterial diseases (5) and are known to carry Campylobacter spp. (6)(7)(8)(9)(10). Vector fl ies can transmit Campylobacter spp. from outside farm livestock to broiler fl ocks because large numbers of fl ies may enter broiler houses by ventilation air (7,11). Our aim was to evaluate the effect of insect screens in addition to existing biosecurity measures against Campylobacter spp. infection of broiler chickens in summer.

The Study
Potential study sites were identifi ed in the Danish Poultry Council´s national surveillance database (3) on the basis of the number of Campylobacter spp.-positive fl ocks produced in broiler houses during 2003-2005. All farms practiced hygiene procedures such as separating clean and dirty zones, changing footwear and clothes, and washing hands with disinfecting soap before entering the broiler room. Furthermore, a 3-m zone with short-cut grass or gravel surrounded the houses. Houses were emptied, cleaned, and dried before each new fl ock of chickens was brought in. All farmers were instructed to maintain biosecurity and management routines as before the study. Case and control groups were assigned to match each other in Campylobacter spp. prevalence and were composed so that the distribution of previous Campylobacter spp. prevalence of fl ocks for each group (June to November during 2003-2005) were equal ( Figure 1) and with similar distribution in the presence of other livestock in a periphery of 1.5 km around the farms. Farmers consented to participate before study groups were composed.
According to data from the national Danish Campylobacter surveillance program (3) Twenty houses on 11 farms in Jutland, Denmark, were equipped with fl y screens by June 1, 2006 (photographs available from www.vet.dtu.dk/default.aspx?id=20832). Fifty-two broiler fl ocks stocked in the houses after June 1 constituted the cases; the last fl ock was slaughtered on November 6, 2006. Controls were 70 broiler fl ocks reared in 25 matched broiler houses on 13 other farms without fl y screens; the last fl ock was slaughtered on November 13, 2006. All houses were ventilated through wall inlets in the long sides of the houses, air outlets through chimneys in the roofs, and gable fans. The study design was based on experience gained in a pilot study in 2004 (11) of 5 farms with parallel case and control houses on each farm. The pilot study showed a signifi cant delay of Campylobacter spp. introduction in case houses. However, only a 37% reduction in positive broiler fl ocks was obtained at slaughter due  to transmission of Campylobacter spp. from control houses to the corresponding case houses. Broiler fl ocks were sampled at days 21, 28, and 35. Boots with over-shoe covers were used to walk through the broiler rooms. The over-shoe covers (photographs available from www.vet.dtu.dk/default.aspx?id=21756) were analyzed for Campylobacter spp. Results are shown in Table 1. Flocks were slaughtered between days 35 and 42 and sampled by collection of 10 cloacal swabs per fl ock at the abattoir. Results of the current national surveillance program of Campylobacter spp. in broiler production were included in the study as reference to ordinary Danish broiler production. All samples were analyzed by PCR (DANAK [The Danish Accreditation and Metrology Fund] accredited method) detecting thermophilic Campylobacter spp. (12).
In fl y screen houses (case houses), 15.4% (95% CI 7.7%-27.8%) of the fl ocks reared during the study period were Campylobacter spp. positive at slaughter, whereas the prevalence in Campylobacter spp.-positive fl ocks reared in the control houses was 51.4% (95% CI 40.0%-62.7%). The prevalence in the control houses remained unchanged (p = 0.68 by χ 2 test) compared with the historical prevalence during June-November, 2003-2005. Figure 1 shows the Campylobacter spp. prevalence of fl ocks from the study with the historical data. The average fl ock Campylobacter spp. prevalence per month in 2006 in fl y screen houses and in control houses is shown in Figure 2 with the results of the national Danish Campylobacter surveillance program of 1,504 broiler fl ocks slaughtered in Denmark in specifi c months.
Data were analyzed with SAS software (SAS Institute, Cary, NC, USA) in the SAS procedure proc genmod with a logit link function and a repeated statement where subject = fl ock. The repeated statement accounts for the intraclass correlation. In the model, the effects of the fl y screen "Screen" of the time between 21 and 35 days "Time", the interaction "Screen Time" and the effect of the average monthly prevalence level at slaughter "Month" (analyzed as regressor) were analyzed. The status at day 35 was chosen in the analysis instead of the results at slaughter to avoid biases in data due to the increased risk of introducing Campylobacter spp. in those fl ocks slaughtered later and during depopulation and transportation to slaughter. Only 4 fl ocks were slaughtered during November and were merged with the October fl ocks in the analysis.  Table 2.

Conclusions
We showed that preventing fl ies from entering broiler houses in the summer of 2006 caused a drop in prevalence of Campylobacter spp.-positive fl ocks at slaughter from 51.4% in control houses to 15.4% in case houses. It seems reasonable that the main results found in this study can be extrapolated to the national situation because the selected control houses had a prevalence similar to the national prevalence level for the same period ( Figure 2). Installation of effective fl y screens in broiler houses in Denmark would most likely decrease the average yearly Campylobacter spp. prevalence, and show a major decrease in the summer peak. Presumably, the risk for infection from eating chicken, the main cause of campylobacteriosis in Denmark (13), would be reduced. The expected effect on the incidence of chicken-borne campylobacteriosis has been calculated by Rosenquist et al. (14) to be proportional to the decline in fl ock Campylobacter spp. prevalence.
Our study provides evidence that fl ies are vectors for Campylobacter spp. in broilers and furthermore, probably explains the seasonal variation of Campylobacter spp. in   chicken products. Flies may also play a role in direct transmission of Campylobacter spp. to humans (14,15). Certainly, the issue deserves further scientifi c investigation. All material published in Emerging Infectious Diseases is in the public domain and may be used and reprinted without special permission; proper citation, however, is required.