Lairage is a Hazard for Salmonella Contamination in the Pork Chain

H. Scott. Hurd1, J.D. McKean2, R.W. Griffith2, I.V. Wesley1, M.H. Rostagno1, J.K. Gailey1, L.A. Karriker1
1National Animal Disease Center, ARS, USDA. Ames, Iowa
2College of Veterinary Medicine, Iowa State University. Ames, Iowa


The pork industry is concerned about Salmonella contamination in pork. As one packing company executive stated, “The food safety issue is a matter of life and death for our industry… Food safety must come first, above all other issues, including productivity and profitability.” However, the industry still needs proven control methods. Pork plants have the lowest HACCP compliance rates; lower than poultry, ground beef, or cow and bull products (FSIS 2000). For small plants only 47% of carcass sample sets, collected in 1999, met the current standard of 8.7% Salmonella prevalence. Producers also recognize the importance of reducing Salmonella, but are limited by lack of clear interventions steps. This area has been a major focus of our research group for the past three years.


Many researchers have reported a higher Salmonella prevalence for pigs tested at slaughter, compared to when they are tested on-farm (Morgan et al., 1987; Berends et al, 1997). Virtually all pigs must be transported and most are held for at least two hours after transport, to improve meat quality (Berg 1999). Considerable evidence is accumulating that much Salmonella infection is occurring in the last few hours of life. The antemortem holding pens appear to be the primary source of this preharvest infection. This report will summarize the accumulated evidence that lairage, as currently practiced in the USA, is a significant Salmonella hazard. This information has substantial impacts on the strategies that can be successful in reducing Salmonella contamination of pork.


No direct effect of stress


The stress of transport has been suggested as a reason for increased S. enterica shedding from farm to market. The physiological changes associated with stress might encourage the recrudescence of latent carriers or it might increase the susceptibility of noncarriers to new infection. However, no studies have demonstrated a direct increase in S. enterica shedding or infection due to these physiological changes.


In support of this hypothesis, we demonstrated no difference between directly shipped pigs and those stressed by mixing, fasting and 18 hours lairage in a clean disinfected facility (Hurd et al. 2001a). After transport and 2 hours holding at the abattoir, control (farm direct) animals had higher isolation rates than did pigs held for 18 hours, transported, and held 2 hours (78.3% vs. 65.2%). Figure 1 compares fecal and colon isolation rates for direct shipped and lairaged (18 hours) animals. Only 3.4% of these pigs were positive by fecal culture on-farm. A single Salmonella enterica serotype (Derby) was identified on farm over the 10 week study period.


However, less than 24 hours later, 71% of these pigs were positive when culturing various slaughter samples. Additionally, 17 different serotypes were identified, over the 10 week study period. Interestingly, the predominant serotype varied weekly through the 10 sampling weeks (Agona and Anatum, week 1; Derby, week 2; Typhimurium, week 3 & week 6; Manhattan, week 8; Uganda, week 9).


This field study utilized 300 market swine from a single pork-production facility. Thirty pigs were tested at the production site during each of the 10 sampling periods. Half of tested pigs were moved to a clean and disinfected holding facility for ~18 hours before both groups were transported to a commercial high-capacity (16,000 head/day) abattoir. After slaughter, carcass swabs, ventral thoracic and subiliac lymph nodes, and various intestinal tissue samples were cultured for Salmonella.



Evidence for a non-farm source of infection


To standardize the samples collected on-farm and at the abattoir, we conducted another study and found more evidence that the holding pens were a significant source of Salmonella infection (McKean et al. 2001; Hurd et al. 2002). As with the lairage study, the number of different serotypes isolated was much higher for those samples collected at the abattoir (n=17) compared to the farm (n=8). More serotypes were isolated from pigs necropsied at the abattoir than were not found in pigs necropsied on-farm, even though the same tissues were collected at both locations.


For abattoir necropsied pigs, the average Salmonella prevalence was seven times (39.9%) higher than on-farm collected samples (5.3%) (P < 0.001). Figure 2 compares isolation rates for on-farm and abattoir collected samples by sample type (fecal, cecal contents, lymph nodes).


We conducted this study using six Iowa herds enrolled in the Accelerated Pseudorabies Eradication Program (APEP). Market pigs (pen-mates) were randomly assigned 48 hours before depopulation to be necropsied either on the farm of origin or at the abattoir, after transport in disinfected trailers and 2-3 hours holding. The same samples (1g feces, ileocecal lymph node, cecal content, superficial inguinal lymph node) were collected at both locations. Abattoir collected samples were obtained, before entry on to the kill floor, by the same necropsy methods as used on-farm.


Figure 2. Percent pigs Salmonella positive by sample collected at abattoir and farm necropsy

Figure 2. Percent pigs Salmonella positive by sample collected at abattoir and farm

Rapid infection is possible


The previous studies pointed to the possibility of rapid infection after pigs left the farm. To determine if rapid infection, via oral exposure, was feasible, we conducted two experiments at the USDA National Animal Disease Center. The first experiment demonstrated that market swine can become infected in the ileocecal lymph nodes and gastrointestinal tract after only 2 hours of exposure to a Salmonella contaminated floor (80% positive) (Hurd et al. 2001b). A follow up study showed that intestinal contamination, without lymph node invasion, can occur 30 and 60 minutes after exposure (50% positive) (Hurd et al. 2001c).


Most (80%) of the animals necropsied after 2 hours exposure were positive for the marked strain. After 3 hours, 60% of the pigs were positive. One pig even had a positive mandibular lymph node. After 6 hours, all (100%) of the animals had at least one tissue sample test positive. At 30 and 60 minutes 50% of the necropsied pigs were culture positive in the cecum, ileum or rectum. Compared to other experimental inoculation studies, the exposure dose of Salmonella was relatively low, (1.5 X 103 CFU/gram of feces).


These experiments were designed to simulate the exposure at the antemortem holding pen. Crossbred market weight swine (~92kg) were exposed to feces containing a marked (nalidixic acid resistant) strain of Salmonella enterica Typhimurium. The contaminated feces were deposited on the floor by two pigs that had been intranasally inoculated 4 days previously.


These shedding pigs were then removed and Salmonella negative pigs placed in the room with feces remaining from the shedders. Exposed pigs were autopsied after 2, 3 and 6 hours of exposure; or 30 and 60 minutes in second experiment.


Holding pens are Salmonella contaminated


In another study, we demonstrated that the holding pen environment is highly contaminated with Salmonella (Rostagno, et al., 2001). Similar results have been reported from the Netherlands (Swanenburg, 2001). In two typical midwestern high-capacity pork-processing plants (7,800- 16,000 head/day), we isolated Salmonella from 100% of pens tested; 33% of waterers were Salmonella positive. One half of these pens had been high-pressure washed before sample collection.


We also compared the Salmonella serotypes isolated from: 1) the pens before study pigs were placed, 2) the truck floors after shipping and unloading, and 3) slaughter tissues collected from these study pigs. Serotype diversity analysis indicates that pigs are picking up new serotypes from the pens. In the pig tissues, twenty-six percent of samples from study pigs contained Salmonella serotypes found only in the pens but not in the trucks; demonstrating that pens can serve as a ready infection source.


Further evidence and future work


Preliminary analysis of a recently completed study in cull sows showed that time spent in holding pens increased Salmonella prevalence, regardless of transport. In this study sows were collected from a buying station, transported 6-8 hours and randomly assigned to immediate harvest or 2 hours wait in the holding pen before harvest. Salmonella was isolated from 57% of sows held in the pens compared to 43% not held in the pen (P < 0.05).


Future work will compare holding and no-holding in market pigs. Additionally, future work will investigate pen contamination levels and seasonal variations, and try to develop economical pen level interventions to reduce contamination.


This summary presents reasonable evidence that lairage (holding), as currently practiced in the USA (and most of the developed world), is a significant hazard for Salmonella infection and contamination in pork. This research presents new possibilities for control. Effective reduction of Salmonella at the antemortem holding pen should decrease the risk of Salmonella contamination at later steps in the pork production chain. Since antemortem pens are a source of Salmonella for all incoming swine, this potential control point must be addressed before on-farm reduction can be expected to reduce pork contamination.



Berends, B.R. Urlings,H.A.P. Snijders, J.M.A. Van Knapen, F. 1997. Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. International Journal of Food Microbiology, 30:37-53.
Berg, EP 1999. Critical Points Affecting Fresh Pork Quality within the Packing Plant, NPPC Fact Sheet, Des Moines, Iowa.
FSIS 2000. Progress Report on Salmonella testing of raw meat and poultry products. USDA Food Safety Inspection Service. March 2000.
Hurd, H.S., McKean, J.D., Wesley, I.V., et al. 2001a. The effect of lairage on Salmonella
isolation from market swine. J Food Prot 64 (7): 939-944.
Hurd, H.S., Gailey, J.K., Rostagno, M.H. 2001b. Rapid infection in market swine following exposure to a Salmonella contaminated environment. Am J. of Vet Research. 62(8):1194-1197.
Hurd, H.S., McKean, J.D., Gailey, J.K., Rostagno, M.H. 2001c. Experimental rapid infection in market swine following exposure to a Salmonella contaminated environment. Berliner Müchener Tierärztliche Wochenschrift 114(9/10):382-384.
Hurd, H.S., McKean, J.D., Griffith, R.W., Wesley, I.V., Rostagno, M.H. 2002. Salmonella enterica infections in market swine before and after transport and holding. Applied and Environmental Microbiology. 68:5 2376-2381.
McKean, J.D., Hurd, H.S., Rostagno, M.H., Griffith, R.W., Wesley, I.V. 2001. Transport and holding at the abattoir: A critical control point for Salmonella in market swine? Proceedings of the 4th International Symposium on Epidemiology and Control of Salmonella and other Foodborne Pathogens in Pork. Leipzig Germany, September 2-5, 2001 p. 292- 294.
Morgan, I.R., Krautil, F.L., Craven, J.A. 1987. Effect of time in lairage on caecal and carcass Salmonella contamination of slaughter pigs. Epidemiol Infect 98:323-330.
Rostagno, M.H., Hurd, H.S., McKean, J.D., Ziemer, C., Leite, R.C. 2001. Abbatoir holding pens as a source of Salmonella for swine. Proceedings of the 4th International Symposium on Epidemiology and Control of Salmonella and other Foodborne Pathogens in Pork. Leipzig Germany, September 2-5, 2001, pp 298-300.
Swanenburg, M., H. A. P. Urlings, D. A. Keuzenkamp, and J. M. A. Snijders. 2001. Salmonella in the lairage of pig slaughterhouses. J. Food Prot. 64:12-16.


Dr. Scott Hurd
Dr. Hurd received his D.V.M. from Iowa State University in 1982 and his Ph.D. from Michigan State University in 1990. Current position: Analytical Epidemiologist, Preharvest Food Safety and Enteric Diseases Research Unit, National Animal Disease Center: ARS: USDA.