IMPACT OF TRANSPORT AND RELATED STRESSES ON THE INCIDENCE AND EXTENT OF HUMAN PATHOGENS

IN PIGMEAT AND POULTRY

R.W.A.W. MULDER

DLO-Institute for Animal Science and Health (The former Spelderholt Centre for Poultry Research and Information Services)

Agricultural Research Department @LO-NL) P.O. Box 59, 6700 AB Wageningen, The Netherlands

Accepted for Publication June 27, 1995

ABSTRACT

Meat products are very important sources of protein in the human diet. The contamination of these products with pathogenic microorganism, such as Salmonella and Campylobacter, make both production and consumption of them a precarious proposition. Several methods can decrease the level of contamina- tion with these pathogenic microorganisms. However, there are still situations of high microbial load which cannot be explained and are ofen attributed to stress. This paper describes the effect of transport, husbandry and nutrition practices on contamination of slaughtered products. Examples of the stress occurring during fattening, catching and loading, transport and conditioning at the processing plant, are given.

INTRODUCTION

Meat forms an important component in the Western diet. Over the years, there have been increasing requirements from consumers for foods that are safe, do not need the addition of preservatives and need little or no preparation or cooking by the consumer. Thus there is a real pressure to produce meat and meat products that contain minimal numbers of both spoilage and human pathogenic organisms.

Human foodborne diseases are considered to be one of the major problems in the modem world, and they are an important cause of economic losses due to hospitalization and absenteeism. Salmonella and Campylobacter infections account for the majority of acute cases of human gastroenteritis. The results of sentinel and population studies (Table l), carried out in The Netherlands since 1987, demonstrate that Campylobacter bacteria are the most prominent cause of acute gastroenteritis in humans. This seems in contrast to traditional reports,

Journal of Food Safety 15 (1995) 239-246. Aff Rights Reserved. OCopyright 1995 by Food & Nutrition Press, Inc., Trumbull, Connecticut. 239

240 R.W.A.W. MULDER

where Salmonella is the top-seeded organism. This difference is probably caused by the past (and in some cases continued use) use of investigating and reporting systems, that do not include Campylobacter.

Salmonella spp., Campylobacter spp., Listeria monocytogenes and Staphylococcus aureus are the potentially pathogenic microorganisms which are most frequently isolated from live animals and pig and poultry meat.

TABLE 1 . CAUSES AND INCIDENCES OF ACUTE GASTROENTERITIS IN MAN

IN THE NETHERLANDS 1987-1992

Incidence

Microorganisms (X) per year) Frequency (#/lo00 individuals

Campylobacter Salmonella Shigella Escherichia coli Clostridium perfringens Rotaviruses

12-15 4-5 0-3

3 3 6

18-23 6-11

Adapted from Notermans and van de Giessen (1993).

Although the reports of isolations are not consistent for all organisms from all commodities, some trends can be observed. Salmonella isolations are most frequently reported; the most important Salmonella serotypes in isolates from humans, poultry and pigs are shown in Table 2. Unfortunately, comparable data are not available for Campylobacter and other pathogenic microorganisms. From these results, it is evident that even in a two year period the top-five Salmonella serotypes have changed. In 1985, S. enteritidis accounted for approx 2.4% of the human isolates in The Netherlands. In 1989 this figure was 20.1 % and rose to 34.4% of the isolates in 1991. The data in Table 2 also suggest that S. typhimurium infections in humans are caused by pigs, and S. enteritidis infection by poultry.

In a recent survey, Jacobs-Reitsma et al. (1994), estimated the Cumpylob- acter and Salmonella incidence in broiler flocks over a one year period from early 1992 to early 1993. Campylobacter spp. were isolated from 153 out of 187 broiler flocks (82 %). Campylobacter jejuni was the dominant species, although due to novel serotyping systems the difference with C. coli isolates is not very

HUMAN PATHOGENS IN PIG AND POULTRY 24 1

clear. There was a seasonal variation with maximum isolation rates in June- September and minimum isolations in March. In the same flocks the Salmonella contamination was not influenced by the season and Salmonella was isolated from 49 out of 181 flocks (27%). Consumer-ready poultry products were Campylobacter-positive in 62.6 % of the samples and Salmonella-positive in 44.2% of the total number of samples (Bolder 1993).

TABLE 2. TOP FIVE SALMOh'ELLA SEROTYPES IN ISOLATES FROM HUMANS,

POULTRY AND PIGS IN THE NETHERLANDS

Human (%) Poultry (%) Pig (%) 1989 1990 1989 1990 1989 1990

S. typhimurium 44.9 39.7 16.9 18.4 81.2 77.6 S. enteritidis 20.1 29.5 19.5 10.0 1.0 < 1 S. virchow 6.2 6.8 8.6 13.1 < I 0 S. hadar 2.2 2.6 9.9 18.8 0 < 1 S. infantis 2.4 1.9 11.3 14.2 1.9 1.5

Data: National Institute of Public Health and Environmental Protection, Bilthoven, The Netherlands

In contrast to poultry, where Campylobacter jejuni is the predominant species, pigs are believed to be the most important source of Campylobacter coli. Faecal carriage rates of Campylobacter spp. among pigs may be as, in poultry, up to 100%. Contamination of slaughter pigs before chilling is up to 30 % , after overnight chilling this is below 3 % . The treatment of pigs before slaughter influences contamination of pig products with these organisms. The length of stay in lairage is an important factor in reducing Salmonella contamination of pig products (Morgan er al. 1987).

The reduction of contamination of live animals with Salmonella and other potentially pathogenic microorganisms has been the subject of study in many countries over the last 25 years. Until now no single treatment or process able to eradicate Salmonella and other pathogens could be identified. Even the mechanism of infection with these organisms could not completely be elucidated for all potentially pathogenic microorganisms. The use of competitive exclusion has been somewhat successful. The treatment of day-old broiler chicks with a microbiota which colonizes them and confers resistance to colonization by pathogens, the so-called competitive exclusion treatment, reduces the contamina- tion of flocks by Salmonella and Campylobacter under laboratory and farm

242 R.W.A.W. MULDER

conditions. In studies where flocks were also transported to the slaughterhouse and examined again for these microorganisms, higher contamination rates were found (Goren er al. 1988). Similar results were reported for pigs. The collection of the animals on the farm, their transport to the processing plant and the holding time and conditions before slaughtering seem to induce the spreading of organisms, resulting in higher contamination and a continued carrier state of the animals.

Salmonella and other pathogenic microorganisms may be transferred from one animal to another when they are waiting slaughter, via faeces and drinking troughs. The prevention of an excessively long period of holding in lairages and prevention of overcrowding, specially in pigs, will considerably reduce the proportion of animals found contaminated at slaughter. Clinically healthy ani- mals carrying Salmonella and other pathogenic microorganisms may change their excretion pattern of the organisms from intermittent to constant shedding if an external factor upsets the equilibrium of their intestinal flora. A disturbance of the intestinal functions will lower the resistance of the live animal and facilitates the spreading of intestinal bacteria.

“Stress” is the word often used in those situations which are too complex to be understood, and it is often used to explain why preventive measures to control spreading of pathogens in live animals do not work. Stress factors described in the literature were observed during fattening, catching and loading, transport and conditioning. Stress can, among others, be accompanied by symptoms such as damage to the intestinal tract and a lower capacity of the immune system.

The influence of stress on the immune system is complex and depends on a number of factors. Among these are: the stressor, genetics, nutrition, antigen concentration. Some stressors are believed to influence positively the resistance to infections with pathogens. Examples are some forms of so-called social stress which seem to increase resistance against S. aureus and E. coli. On the other hand, other social stressors, for example mixing pigs from different herds together at transport, have resulted in higher rates of contamination in pigs. (Williams and Newel1 1968; Gallwey and Tarrant 1979). Renwick et al. 1993, recently, demonstrated, that products became more contaminated with microor- ganisms when the time between crating and holding before slaughter increased. This indicates shedding of faecal material, which spreads over live birds. The number of hours of feed withdrawal prior to crating also influences excretion of pathogens. Normally chickens empty their caeca every 24 h, but because of the change in environmental conditions the excretion pattern changes. In the literature most data relate to spreadinghhedding of Salmonella bacteria. Although Campylobacfer seem to cause more problems with regard to human public health, this prominent position is not reflected yet in the literature.

HUMAN PATHOGENS IN PIG AND POULTRY 243

EXAMPLES FROM PIGS AND POULTRY

Pigs

Preslaughter handling can affect the contamination rate of slaughtered animals. Feeding, environmental conditions during transport and lairage, inclu- ding the total time involved and mixing animals from several herds, are the main factors. Slavkov ef al. (1974) demonstrated the effect of stress during loading, transport and holding time before slaughter. Before pigs were delivered to the abattoir, none were isolated; after delivering to the abattoir 0.1 % (2/1952) of the samples were positive; after slaughter this percentage increased to 0.7%. The authors conclude, that stress factors had been responsible for the increase in the carrier state.

The most comprehensive work in this area is by Morgan el al. (1987). These authors studied the effect of time spent in lairage on caecal and carcass Salmonella contamination of groups of pigs originating from one producer and slaughtered in two different abattoirs. The main differences between the abattoirs were pen size and (visual) hygiene (abattoir 1: larger pens and less hygiene). Table 3 presents some data from this study. Thus the time spent in lairage can be used to minimize Salmonella contamination. The shorter the period, the better. Pen size (smaller pens) and hygiene are the other important factors to decrease (cross)contamination. In this study carcass contamination was caused by intestinal Salmonella infections. This could be demonstrated by the Salmo- nella recovery rate and the Salmonella serotypes from caecal contents and the carcass surface.

TABLE 3. ISOLATION OF SALMOh'ELLA FROM CAECAL CONTENTS OF PIGS HELD IN

LAIRAGE FOR THREE DAYS (18,42 AND 66 H) IN TWO ABAnOIRS Number of positivesltotal number sampled.

Caecal isolation rate

Abattoir Day 1 Day 2 Day 3

1 2

20175 29/71 45/75 8/76 6/74 24/74

Total 28/151 351145 711149 (18.5%) (24.1 %) (47.7%)

Adapted from Morgan et nl. (1987).

244 R.W.A.W. MULDER

As carcass contamination was determined by the Salmonella entering the abattoir in the intestine of the pigs, a very important strategy to reduce contamination is preslaughter handling avoiding any form of multiplication of Salmonella in the live animals (see also Huis in’t Veld et al. 1994). Another reason for spending a short time in lairage, is the economic aspect of the carcass weight loss with increasing time.

Poultry

Stress in poultry is accompanied by a series of symptoms. The increased corticosteroid levels in blood plasma and the occurrence of damage to the intestinal tract, heart and blood vessels are of major importance. Decreased shear strength of the intestinal tract may result in gut breakage during processing, which is responsible for further spreading of microorganisms over carcasses and equipment (Bilgili 1988). Feed and water withdrawal prior to transport, influences gut contents and the emptying of the digestive tract of broilers. Papa and Dickens (1989) concluded that feed withdrawal 8-12 h before slaughtering minimizes the faecal contamination of carcasses. Moran and Bilgili (1990) demonstrated that stressing chicken broilers, under conditions simulating the practice of feed withdrawal and live haul, results in a delayed caecal retention for another 24 h.

Bolder and Mulder (1983) reported the increase of Salmonella contamination of slaughtered broilers after transport. The similarity with findings in the pig industry, as in other areas, is striking: Salmonella serotypes after transport observed on slaughtered products originate from live birds, which indicates intestinal origin. The question arises whether there is not a major discrepancy between husbandry and nutrition factors aiming at the economical production of poultry broilers and the contamination of consumer-ready products with potentially pathogenic microorganisms. Preslaughter conditions influence the contamination rate of slaughtered products. However, the real circumstances and mechanisms are not known. To interrupt microbial cycles in animal production, more attention should be paid to aspects of contamination in relation to husbandry, nutrition and processing, including conditions of loading and tran- sport.

CONCLUSIONS

The mechanism of spreadinghhedding of microorganisms from clinically healthy carrier animals under stressing conditions is not clear. Nevertheless from the literature and actual practice, it is known that preslaughter conditions in handling live animals influence the contamination rate of the slaughtered product. Therefore preloading activities in the shed, the loading procedure, the

HUMAN PATHOGENS IN PIG AND POULTRY 245

transport, the holding period and conditions at slaughter and the slaughter process itself should be given more care.

REFERENCES

BILGILI, S.F. 1988. Effect of feed and water withdrawal on shear strength of broiler gastro-intestinal tract. Poultry Sci. 67, 845-847.

BOLDER, N .M. 1993. Salmonella, Campylobacter, Listeria and Escherichia coli 0157:H7 monitoring in Dutch poultry products on retail level. Spelderholt Confidential Rept. 695-15.

BOLDER, N.M. and MULDER, R.W.A.W. 1983. Contamination des carcasses de poulets pas des Salmonelles: Le role des caisses de transport. Courr. Avicole 39, 23-25.

GALLWEY, W.J. and TARRANT, P.V. 1979. Influence of environmental and genetic factors on the ultimate pH in commercial and pure-bred pigs. Acta Agric. Scandinavica Suppl. 21, 32-38.

GOREN, E., DE JONG., W.A., DOORNENBAL, P., BOLDER, N.M., MULDER, R.W.A.W. and JANSEN, A. 1988. Reduction of Salmonella infection in broilers by spray application of intestinal microflora: a longitudi- nal study. Vet. Q . 10, 249-255.

HUIS IN’T VELD, J.H.J., MULDER, R.W.A.W. and SNIJDERS, J.M.A. 1994. Impact of animal husbandry and slaughter technologies on microbial contamination of meat: monitoring and control. Meat Sci. 36, 123-154.

Campylobacter and Salmonella in broiler flocks. Intestinal carriage of Campyobacter and Salmonella in Dutch broiler flocks at slaughter: a one- year study. Poultry Sci. 73, 1260-1266.

MAY, J.D. and DEATON, J.W. 1989. Digestive tract of broilers cooped or deprived of water. Poultry Sci. 68, 627-630.

MORAN, JR., E.T. and BILGILI, S.F. 1990. Influence of feeding and fasting market age broilers on cecal access to an oral dose of Salmonella. J. Food Prot. 53, 205-207.

MORGAN, J.R., KRAUTIL, F.L. and CRAVEN, J.A. 1987. Effect of time lairage on caecal and carcass Salmonella contamination of slaughter pigs. Epidemiol. Infect. 98, 323-330.

NOTERMANS, S . and VAN DE GIESSEN, A. 1993. Foodborne diseases in the 1980s and 1990s. Food Control 4, 122-124.

PAPA, C.M. and DICKENS, J.A. 1989. Lower gut contents and defecatory responses of broiler chickens as affected by feed withdrawal and electrical treatment at slaughter. Poultry Sci. 68, 1478-1484.

JACOBS-REITSMA, W.F., BOLDER, N.M. and MULDER, R. W.A. W. 1994.

246 R.W.A.W. MULDER

RENWICK, S.A., McNAB, W.B., LOWMAN, H.R. and CLARKE, R.C. 1993. Variability and determinants of carcass bacterial load at a poultry slaughter abattoir. J. Food Prot. 56, 694-699.

SIEGEL, H.S. 1987. Effects of behavioural and physical stressors on immune response. In Biology of Stress in Farm Animals: An Integrative Approach, (P.R. Wiepkema and P.W.M. van Adrichem, eds.), pp. 39-55, Martinus Nijhof Publishers.

SLAVKOV, I., IODANOV, I., MILEV, M. and DANOV, V. 1974. Study of factors capable of increasing the number of Salmonella carriers in clinically normal pigs before slaughter. Veterinarnomeditsinski Nauki, Bulgaria, 11,

WILLIAMS, L.P. and NEWELL, K.W. 1968. Sources of salmonellae inmarket 88-91.

swine. J. Hyg. 66, 281-293.