Objectives, Program, and Effects

The initial aim of the program was that <5% of broiler flocks would be infected with Salmonella. The program was successful and was gradually revised towards assurance of complete freedom from Salmonella in broiler production.

The program is based on the principle of top-down eradication, ensuring freedom from Salmonella from the top of the broiler-breeding pyramid down. Infected flocks of breeding animals are destroyed, and infected birds are processed for slaughter. The testing program has developed gradually to adjust to higher food safety objectives. As progress stalled, more intensive serologic and bacteriologic testing was developed and applied (5,9–11). The current testing scheme is shown in Table 1.

Birds from infected flocks are slaughtered on separate slaughter lines or late in the day to avoid cross-contamination. Farmers get a better price for birds from Salmonella-free flocks, and slaughterhouses can use the label “Salmonella-free” for birds that meet criteria determined by the authorities. No decontaminants, such as organic acids or chlorine, are used during carcass processing.

Figure 1

Figure 1. Salmonella in Danish broiler flocks as determined by bacteriologic testing of every flock 2–3 weeks before slaughter (N>4,000 flocks/year).

The proportion of Salmonella-infected broiler flocks has been markedly reduced since the initiation of the control program. Figure 1 shows that >65% of broiler flocks tested positive for Salmonella during the first year of the program, 1988–89, versus <5% in 2000. This decrease in Salmonella has led to a concomitant reduction in the proportion of infected broiler carcasses after slaughter and at retail.

The Danish government and the European Union equally compensate owners of destroyed breeding stock for their losses. In 1993, a major Danish retailer (COOP-Denmark) stopped the marketing of broiler chicken, which exceeded a 5% target. Danish chicken could not meet this target at that time, so producers suffered severe losses because they had to export their chicken to lower priced markets.

Salmonella can be effectively reduced (nearly eliminated) from broiler chickens by intensive flock-level testing and top-down eradication. Essential to success is a sufficiently sensitive testing program in the breeding and rearing flocks as well as in the hatcheries, i.e., one that involves intensive sampling and a combination of serologic and bacteriologic testing methods (Table 1). Bacteriologic testing alone is not sufficiently sensitive to achieve control, especially if S. Enteritidis infections are present. Removal of all organic material, thorough cleaning and disinfection of the poultry house, and an empty resting period of 10–14 days between flocks can effectively eliminate residual infections. In Denmark, most infections appear to be vertically transmitted (nearly always traceable to an infected hatchery or parent flock), whereas horizontal transmission from the environment and wild fauna appear to play a minor role. Competitive exclusion cultures, vaccines, or antibiotics have not been used in the Danish control program.

Objectives, Program, and Effects

Figure 2

Figure 2. A) Receipt of 60 eggs per producer every 9 weeks (barcode indicating producer is shown). B) The “eggbreaker” punches a hole in 30 eggs at a time. C) Withdrawal of egg...

All shell eggs from commercial layer flocks should be free from S. Enteritidis and S. Typhimurium. Control of layer breeders in Denmark is essentially identical to the control program for broiler breeders (Table 1). Blood and fecal samples of rearing flocks are tested (8,11), and infected flocks are destroyed. All commercial flocks of layer hens in production are tested routinely every 9 weeks by a combination of serologic testing of egg yolk and bacteriologic testing of environmental samples (Table 1, Figure 2).

All eggs from suspect or confirmed-positive layer flocks are pasteurized. All shell eggs are distributed in a cold chain (not exceeding 12°C) and kept refrigerated at retail; eggs are generally refrigerated in private homes.

Figure 3

Figure 3. Salmonella in Danish layer flocks as determined by serologic and bacteriologic testing of each commercial flock in week 9 of production.

The government and the European Union equally compensate owners of destroyed breeding stock for their losses. The proportion of layer flocks infected with Salmonella, notably S. Enteritidis, has been markedly reduced since the initiation of the control program. Figure 3 shows that >7% of layer flocks tested positive for Salmonella in the first year of the program, 1998, versus <2% in 2001. The level of Salmonella-contaminated shell eggs has not been measured from the initiation of the control program. However, a year before the program began, a study of 13,000 eggs from different types of production determined the level to be 1 per 1,000 eggs (20% of the contaminated eggs harbored S. Enteritidis) (12).

Top-down eradication of S. Enteritidis has effectively reduced the level of Salmonella, notably S. Enteritidis, in Danish commercial layer flocks. The program has been effective in free range, deep litter, organic, and caged birds. Frequent testing by a combination of serologic and bacteriologic testing methods is essential to achieve adequate sensitivity in the monitoring program. Control of residual infections in poultry houses can be conducted with a success rate of nearly 70% by thorough cleansing and disinfection of the depopulated house (removal of all organic material, disinfection of surfaces, and resting of the empty house for 2 weeks). Day-old chicks for rearing must be antibiotic free. Competitive exclusion cultures and vaccination are not used in the Danish program. Vaccination cannot, at present, be used in combination with serologic testing because of problems of cross-reaction.

Objectives, Program, and Effects

Denmark is the only country with a nationwide control program of Salmonella in pork that is integrated from “feed-to-food.” The program is based on routine testing and classification of slaughter pig herds and subsequent slaughter of pigs according to the inherent risk, as measured by the continual test program (Figure 2; Table 2). The program has been described in detail elsewhere (7,8,13).

Pre-Harvest Control

Figure 4

Figure 4. A) Receipt of pork samples from the slaughterhouse. Each tube is labeled with a barcode, indicating herd of origin. Samples are frozen overnight. B) The tube is entered in a rack...

Pigs from breeding and multiplying herds are tested monthly by serologic testing of blood samples. If a specific cutoff level is reached, bacteriologic confirmatory testing is carried out. Further, if the serologic reactions exceed a specific high level, all movement of animals is restricted. Slaughter pig herds are monitored continuously by serologic testing of “meat juice” (drip fluid released from meat after freezing and thawing) (14). Meat samples for testing are collected at the slaughter line, and the number of samples and frequency of sampling are determined by the size of the herd. Approximately 700,000 slaughter pigs are currently tested each year (Figure 4). Herds sending <200 pigs to slaughter each year are not tested, leaving 1.6% of the slaughter pigs outside the monitoring scheme. The herds are categorized in three levels based on the proportion of seropositive meat juice samples during the last 3 months. Owners in level 2 and 3 are encouraged to seek advice on how to reduce the Salmonella problem in the herd (e.g., feeding, hygiene, and management). Furthermore, payment from the slaughterhouse is reduced by 2% and 4%, respectively.

The postharvest surveillance program has been described (8,15,16). Pigs from herds in levels 1 and 2 are slaughtered traditionally without any special precautions. Pigs from level 3 herds can only be slaughtered in special slaughterhouses under special hygienic precautions. Carcasses from level 3 herds are tested for bacteria after slaughter, and if the level of contamination exceeds a certain limit all carcasses from the particular herd have to undergo heat treatment or other risk-reducing processing. All slaughterhouses do routine bacteriologic testing of carcasses according to a sampling plan, which ensures that testing is random and representative of the national swine production (>30,000 samples/year). Slaughterhouses that exceed a certain predetermined level of Salmonella in the routine monitoring of carcasses are obliged to investigate and reduce the contamination problem to an acceptable level.

Figure 5

Figure 5. Prevalence of Salmonella in Danish pig herds as determined by continuous serologic testing of all commercial pig herds (N >700,000 samples tested/year). Herds are categorized in three levels based on the...

Figure 6

Figure 6. Salmonella detected in pork, as determined by continuous randomized sampling of pork end-products from all major national pig slaughterhouses (N >30,000 samples/year).

The prevalence of swine herds in level 2 and 3 respectively, has been steadily reduced since the program began (Figure 5). Bacteriologic testing has indicated that the herd infection level was reduced by 50% (from 14.7% to 7.2% in small herds and 22.2% to 10.4% in large herds) from 1993 (when the program was implemented) to 1998 (17). In the same period, the level of Salmonella contamination in pork products, as determined by the routine monitoring program, was reduced from 3% to <1% (Figure 6).

Because Salmonella eradication in swine herds is difficult because of the continual nature of the production system, reducing the infection level should be the aim of a control strategy. The low infection level in the herds and contamination in the products can likely be reduced further in Denmark. As the contamination level goes below 1%, testing for contamination requires increasingly large numbers of samples and consequently becomes very expensive, which is one reason the sampling plan of herds and products has become more sensitive in recent years. This change in testing sensitivity makes it difficult to compare current and past levels of infection and contamination but is nevertheless a necessity for the continued improvement of the program.

A combination of serologic and bacteriologic testing is essential for the success of the program. Nearly 1 million serologic samples are tested each year. Testing this large number of samples would not be possible because of financial and logistic constraints if the program were to rely on bacteriologic testing alone.

Feeding strategy (e.g., increased coarseness of feed and wet feeding) and improved management (e.g., sectioning and all-in all-out production) and hygiene standards are important elements in the preharvest control efforts. Using commercial prebiotic cultures is not necessary; natural microflora in the feed, especially wet fermented feed, appear to have a protective effect (18).

A reduction of Salmonella in slaughter pig herds has been attained without Salmonella–free breeding herds. However, to ensure the highest degree of consistency in the program, the levels of Salmonella in breeding herds should be kept as low as possible, and infected breeding herds should not be sold to producers of herds of a superior Salmonella status.

Costs of Salmonella Control

The Audit Office of Denmark has evaluated the government spending in relation to the national Salmonella control efforts (22). From 1994 to 1999, the control program for broiler chickens and layer hens involved government finances of a total of 188.1 million Danish kroner (DKK) (U.S.$26.5 million) (U.S.$1.00 = 7.1 DKK). A total of 109.7 million DKK (U.S.$15.45 million) was paid to compensate farmers for destroyed animals; most of the remaining costs were associated with establishing and running the surveillance program. These costs were highest in the initial phase of the layer hen control program in 1997 but have been reduced considerably since then. In 2001, all costs associated with running the program were assumed by the poultry industry (with the exception of governments’ compensation for flocks destroyed according to the European Union Zoonosis Directive). The current control costs for layer hens and broiler chickens are estimated to be in the range of US$4.2 million per year (for 344 broiler producers, producing 135 million broiler chickens year, and 392 shell-egg producers, producing 1 billion shell-eggs per year).

In the initial phase, the Salmonella control program of pigs and pork cost the industry and government a total of U.S.$14 million per year. With the recent revision of the program, the responsibility has been taken over solely by the industry, and operational costs have been reduced to approximately U.S.$8.5 million per year (for 21,000 producers, producing 21–22 million slaughter pigs each year) (B. Pedersen, pers. comm.).

Public Health Economy

Direct health costs (e.g., hospitalization, consulting a physician, and laboratory testing) as well as the costs of lost labor (e.g., loss of production per day away from work) in relation to a case of salmonellosis in Denmark were evaluated as part of a multidisciplinary task force (Korsgaard and Wegener, pers. comm.). For 2001, foodborne salmonellosis cost the Danish U.S.$15.5 million. The estimate is based on an incidence of 54.6 cases per 100,000, and approximately 10% of cases are laboratory confirmed. Assuming that 5% or 20% of cases are laboratory-confirmed changes the estimate to U.S.$25.5 million and U.S.$10.4 million, respectively.

Costs and Benefits

Assuming that salmonellosis associated with each of the major sources would have remained at the precontrol program incidence (and not increased further) (i.e., if no action had been taken to curb the problem), we calculated a hypothetical “no-control” salmonellosis incidence. This incidence would have been 137.5 (pork 22, broiler chickens 30.8, eggs 57.7, and average residual, 27). The societal costs, in the absence of the existing control programs, would thus have been U.S.$41 million per year (assuming 10% of cases are laboratory confirmed). Thus, in 2001, Denmark saved U.S.$ 25.5 million by controlling Salmonella. The estimated annual Salmonella control costs from 2000 and onwards are approximately U.S.$14.1 million. These costs are borne almost exclusively by the animal producers and the food industry, which suggests that the costs are passed on to consumers through higher food prices. Based on the figures above and data on annual production (23), control costs amount to approximately U.S.$0.075/kg of pork and U.S.$0.02/kg of broiler or egg.