Article pp.285-292 du Vol.28 n°4-5 (2008)

(1)

Focus

12

^es

Journées des sciences du muscle

et technologies de la viande (JSMTV) Selected papers from the proceedings of the Meat Science and Technology Symposium

held in Tours (France), October 8-9, 2008

Meat Science and

Technology

Guest editors-in-chief Cécile Berri Michel Duclos

SDA_28_4-5.book Page 283 Vendredi, 26. mars 2010 11:11 11

(2)

(3)

doi:10.3166/sda.28.285-292 SCIENCES DES ALIMENTS, 28(2008) 285-292

FOCUS : JSMTV

Evolution of foodborne hazards:

Campylobacter and Salmonella

G. Salvat

¹

*, M. Chemaly

¹

, M. Denis

¹

, C. Robinault

¹

, A. Huneau

²

, S. Le Bouquin

²

, V. Michel

²

, P. Fravalo

¹

RÉSUMÉ

Évolution des risques sanitaires : campylobacter et salmonelles

Campylobacter et Salmonella sont les deux premières causes de toxi-infections alimentaires en Europe. depuis 2003, l'Union Européenne a mis en place le règlement communautaire 2160/2003/EC dont l'objectif est l'éradication chez les volailles des 5 sérovars de Salmonella les plus prévalents chez l'homme, ainsi qu'une meilleure maîtrise de ceux -ci en production porcine. En France, la mise en place d'une règlementaton spécifique chez les volailles dès 1998 a permis une réduction des salmonelloses humaines de 33% et une réduction annuelle de 21% de SE et de 18% de ST. Si le système drastique de maîtrise des Salmo- nelles mis en place dans la filière volaille (abattage des troupeaux de reproduct- eurs et de poules pondeuses positifs) a prouvé son efficacité, il n'est pour autant pas transposable à la lutte contre Campylobacter. La plupart des plans de maî- trise des Campylobacter existant en Europe sont basés sur une stricte application de mesures de biosécurité et ont à ce jour échoué dans leurs objectfs de diminution de la prévalence de cette bactérie, tant chez les volailles que chez l'homme. Il faut donc repenser les stratégies de lutte contre les toxi-infections humaines ayant les volailles pour origine. parmi les stratégies envisageables à moyen terme, l'utilisation des bactériophages, la vaccination, l'utilisation de pro- biotiques, de prébiotiques, d'acides organiques, ou de flores de barrière ont été envisagées .Les recherches sont toujours en cours dans ces domaines.

Mots clés

Salmonella, Campylobacter, facteurs de risques, éradication, maîtrise.

SUMMARY

Campylobacter and Salmonella are, in most European countries, the two main causes identified as the source agents of food-borne illnesses. In order to control Salmonella in poultry and pig herds, The European Union has implemented the 2160/2003/EC regulation which aims to eradicate the top five human related most prevalent serotypes on poultry production and to improve the control of

1. AFSSA-LERAPP, HQPAP Unit – PO Box 53 – 22440 Ploufragan – France.

2. EBEAC Unit – PO Box 53 – 22440 Ploufragan – France.

* Correspondence: g.salvat@AFSSA.FR SDA_28_4-5.book Page 285 Vendredi, 26. mars 2010 11:11 11

(4)

286 Sci. Aliments 28(4-5), 2008 G. Salvat et al.

those bacteria in pig production. The establishment of a specific regulation in 1998 in France has led to the decrease of human salmonella by 33% with an annual reduction of 21% for SE and 18% for ST. Although the control system currently focused on Salmonella is based on firm epidemiologic data and offers effective means of control (e.g. slaughtering of positive breeder flocks and laying hens flocks), existing information on Campylobacter makes it more difficult to formulate an effective control plan. Most of the existing control plans against Campylobacter in the EU are based upon the implementation of biosecurity measures and failed to lower the prevalence of the bug in both poultry flocks and humans. New strategies will have to be developed in the next future in order to reduce the risk to human related to poultry consumption. Among those strategies, the use of bacteriophages, vaccination, probiotics, prebiotics, bacteriocins, organic acids and competitive exclusion are still under development.

Keywords

Campylobacter, Salmonella, eradication, control, risk factors.

1 – INTRODUCTION

Campylobacter and Salmonella are, in many countries, the two main causes identified as the source agents of food-borne illnesses (EFSA, 2007). France is no exception: a recent study on the morbidity and mortality caused by food-borne illnesses (INVS, 2003) has shown that Salmonella is responsible for approximately 30,000 to 40,000 cases a year, approximately 5,700 to 10,000 of which required hospitalization and 92 to 535 of which resulted in the death of the patient (Vaillant et al., 2005). Similarly, food-borne illnesses related to Campylobacter occur in approxi- mately 13,000 to 17,000 cases per year of which 2,500 to 3,500 require hospitalization and 13 to 18 cases of which result in the death of the patient (Vaillant et al., 2005). Such numbers are clearly troublesome and it is essential that appropriate actions be taken to control these food-borne diseases. European Union Member States are doing so by implementing a regulation (2160/2003/EC) (EU, 2003) and a directive (2003/99/EC) (EU, 2003) the purposes of which are respectively to establish a means to fight and to control food-borne illnesses of animal origin. Although the control system currently focused on Salmonella is based on firm epidemiologic data and offers effective means of control, existing information on Campylobacter makes it more difficult to formulate an effective control plan. This article will summarize the various means that have been implemented for the control of Salmonella and will establish an initial report on their effectiveness as well as assess the level of knowledge and the deficiencies in terms of control of human Campylobacteriosis.

2 – SALMONELLA

Regulation EC 2160/2003 which lists the control measures (for Salmonella) to be implemented by Member States, requires that prevalence be investigated before the regulation is put in application by the different Member States.

(5)

Evolution of foodborne hazards: Campylobacter and Salmonella 287

European prevalence studies that have focused successively on laying hens, broiler chickens, turkeys (breeding and production), fattening pigs, and this year, pig breeding, have enabled a thorough assessment of poultry and pig farms in Europe.

Table 1 summarizes the completed studies on various types of animal productions in France and in Europe.

Table 1

Prevalence of Salmonella in France (Europe) in poultry and pig production (EFSA, 2004, 2007, 2008).

The study of the sanitary situation of French poultry production puts the country in the leading group of European countries with high-level production. Although egg and turkey chains show satisfactory results regarding S. Enteritidis (SE) and S. Typhimurium (ST), the two main serovars responsible for food-borne illnesses, improvements still need to be implemented in both of these food chains.

With regards to the pork chain, the situation is more uneven as results recorded for France do not position it in the lead among the high-level production countries.

This difference between the poultry and pork chains can be explained by the fact that successive national regulations regarding Salmonella control have been implemented in France since 1982 in poultry chains, while pork chain contamination by Salmonella remains a more recent topic of concern and has not yet been the subject of any specific regulation.

The impact of regulations established as mandatory since 1998 on human salmonellosis for breeding and egg laying flocks of the Gallus gallus chain has recently been evaluated by Poirier et al. (2008). This study highlights the fact that the establishment of a specific regulation in 1998 has led to the decrease of human salmonella by 33% with an annual reduction of 21% for SE and 18% for ST.

The notable decrease of SE shows the effectiveness of the control plan that was implemented and the strong relationship between food-borne illnesses caused by SE and egg consumption. As for the pork chain, although it will be necessary to reduce herd contamination, at least for commercial purposes, its impact on food-borne diseases is most likely reduced because of the way the meat is consumed (well cooked).

Prevalence studies regarding risk factors related to the presence of Salmonella have made it possible to establish an updated assessment for laying hens and broiler chickens (table 2).

While the type of breeding (cage/on-floor) and the size of the flocks stay among the main risk factors for laying hens, we note that most of the other risk factors are related to biosecurity measures and their implementation.

Analytical data relative to turkey and pig studies are not currently available. How- ever, previous studies concerning risk factors for the presence of Salmonella in pig

Salmonella spp. S. Enteritidis S. Typhimurium S. Derby Laying hens 17.2% (30.8%) 3.9% (18.3%) 4.3% (2.6%)

Broiler chickens 6.2% (23.7%) 0.2% (10.9%) 0.1% (0.5%) /

Breeding turkeys 1.6% (13.6%) 0.5% (1.7%) 0% (7.5%)

Turkeys for meat 13.3% (30.7%) 3.8% (3.8%) 3.9% (11.3%)

Pigs (lymph nodes) 18.5% (13.9%) / 7.7% (5.6%) 6.5% (2%)

Pigs (carcasses) 18.6% (6.7%) / 8.2% (3.3%) 6.5% (1.6%)

Pigs (serology) 10%*(NA) / / /

Study of raw meat juices for a threshold value of 40%.

NA: Not Available, measurements are not comparable between various Member States.

/: Not documented.

(6)

breeding (Beloeil et al., 2004) have made it possible to establish the following risk factors (table 3).

Table 2

Salmonella risk factors for laying hens and broilers (RR: relative risk; CI: Confidence Interval) (AFSSA, 2006, 2007).

Table 3

Risk factors for Salmonella excretion in fattening pigs (RR: relative risk) (Beloeil et al., 2004).

Factor % S+ RR (CI 95%)

Size of the flock

≥ 30,000

< 30,000

37.5%

12.5%

2.0 (1.3-3.0) 1.0

Hens

Type of breeding Cage On-floor

30.8%

7.9%

3.5 (2.1-6.0) 1.0 Localization

Rhône Alpes Rest of France

37.1%

16.5%

3.0 (1.7-4.5) 1.0 Trucks passing in front of change room or air intake

Yes No

19.6%

14.2%

1.7(1.1-2.9) 1.0 Disassembly of material during disinfection

Yes No

7.4%

15.2%

0.3 (0.2-0.5) 1.0

Chickens

Presence of a rendering container Yes

No

6.8%

16.2%

1.0 2.0 (1.1-3.6) Neighbor intervention during establishment

Yes No

12.2%

8.2%

2.3 (1.3-4.0) 1.0 Water acidification

Yes No

7.7%

10.2%

1.0 2.7 (1.3-5.8)

Factors % S+ RR (CI 90%)

Emptying of container under slotted floors after removal of the sows Yes

No

24.3%

42.6%

1 1.9 (1.1-3.7) Frequency of removal of manure under the sows during lactation

Twice per day or more Once per day or less

26.9%

45.3%

1 2 (1.2-3.1) Positive feed yard before loading of the batch followed

Yes No

51.4%

28.6%

2 (1.2-3.2) 1 Fattening food type

Soupy Dry

26.1%

52.5%

1 2 (1.2-3.2) Seroconversion to Lawsonia intracellularis during second half of fattening

Yes No

48.4%

31.1%

2 (1.2-3.3) 1 PRRS seropositivity at end of fattening period

Yes No

47.9%

26.3%

2 (1.2-3.4) 1

(7)

The risk factors described in table 3 relate mostly to biosecurity, the quality of herd handling and the general state of health of the herd. Another study (Beloeil et al., 2007) related to risk factors of pig seroconversion has shown that, in addition to the factors described above, group antibiotic treatment during the fattening phase created an additional risk (RR : 2.4 ; CI 95%: 1.7-3.4).

In this case, as before, the general sanitary measures applied during herd handling remain essential to improve Salmonella infection control.

The implementation of these basic biosecurity rules is one of the keys of the vol- untary "sanitary charter" to which laying hen breeders have adhered to massively in order to receive slaughtering indemnifications as provided by the Ministry of Agricul- ture when laying-hen and breeding flocks are positive for Salmonella. It is quite possible that the adaptation of this text for pig breeding will lead to the start of progress towards the reduction of Salmonella prevalence in the pork chain.

3 – CAMPYLOBACTER

Although Campylobacteriosis constitutes only the second cause of food-borne illnesses in France (Vaillant et al., 2005), Campylobacter is the zoonotic agent with the highest incidence in Europe (EFSA, 2007). Thus, 176,016 cases of Campylobac- teriosis have been tallied in 2006 (against 167,241 cases of salmonellosis (EFSA, 2007). In spite of this, European regulations currently do not plan for any control measures of Campylobacter in animal species nor the establishment of any microbiological criteria regarding this micro-organism (2073/2005/EC) (EU, 2005). Direc- tive 2003/99/EC is the only legislation that requires the observation of Campylobacter in animal chains. As such, a prevalence study is currently under way for poultry and poultry carcasses.

3.1 Origin of human Campylobacteriosis

Among the potential sources of human Campylobacteriosis, poultry meats remain the main culprit (EFSA, 2007) even though pork and bovine meats (EFSA, 2007) can also constitute potential sources of Campylobacter (table 4).

Table 4

Contamination of poultry, pork and beef meats by Campylobacter in Europe (Years 2002-2006) (EFSA, 2007).

The high contamination levels of poultry meats reflect a high prevalence in live poultry but are also linked to the slaughtering techniques and the presence of skin on a number of poultry products. Contamination during the course of evisceration is partly responsible for the contamination of commercialized poultry carcasses (EFSA,

2006 2005 2004 2003 2002

Chickens 34.6% 30.5% 37.8% 35% 30.2%

Pigs 0.7% 0.3% 1.6% 1.2% 1.4%

Bovines 0.7% 0.9% 0.6% 0.3% 0.3%

(8)

2004). The prevalence is also elevated in live pigs (Payot et al., 2004; Wehebrink et al., 2008) however, on the one hand, it is mainly due to Campylobacter coli, the importance of which is reduced in human contaminations, and on the other hand, the slaughtering technology used on pigs, particularly singeing, allows for a significant reduction in the number of contaminated carcasses (Wehebrink et al., 2008).

Available data for bovines show low levels of contamination in herds and meats.

Regarding the origins of human Campylobacteriosis, the array of assumptions related to poultry meats has been confirmed through a recent study (Denis et al., 2008) in which the genetic profiles of the human, poultry and pig strains were com- pared in a small region.

Poultry however, is not the sole cause of Campylobacteriosis. Water, milk, or contact with contaminated pets can also cause the disease in humans (EFSA, 2004).

A recent retrospective study in France (Gallay et al., 2008) has shown that the consumption of insufficiently cooked bovine meat (OR: 2.86), eating in restaurants (OR : 2.20) or insufficient hygiene of kitchen utensils (OR: 2.12) constituted significant risk factors for Campylobacteriosis in humans. A higher incidence of Campylobacteriosis related to week-end meals has also been proven (Gillespie et al., 2008) which would tend to prove the risks related to party meals, barbecues… during the preparation of which sanitary conditions can be precarious.

While the introduction of a contaminated primary substance in the kitchen cre- ates an entry for the agents responsible for human Campylobacteriosis, contaminated products handled under insufficient sanitary conditions contribute to the dissemination of Campylobacter in food after its thermal treatment and therefore its recontamination. Quantitative risk evaluation models for Campylobacter highlight the role of sanitary conditions in the kitchen as one of the causes of exposure of the consumer (Rosenqvist et al., 2003). Furthermore, recent studies have shown that the transfer of Campylobacter from chicken skins to work surfaces in the kitchen were possible at rates that were not negligible (from 0.05% to 36%) (Fravalo et al., 2008), as well as to the hands of users (2.9% to 3.8%) (Luber et al., 2006).

Thus it appears that a 2 Log reduction of the number of Campylobacter present on carcasses is an important objective which would have positive results on reduc- ing consumer exposure (Lindqvist et Lindblad, 2008; Brynestad et al., 2008; Rosen- qvist et al., 2003).

3.2 Prevention of poultry contamination by Campylobacter

While the objectives for Campylobacter eradication remain illusory in animal chains in the current state of knowledge, decreasing animal excretions before slaughtering which would then result in decreasing carcass contamination can be contemplated. Several strategies have been evaluated in this regard:

– Treatment or prevention of colonization through the administration of bacterial viruses (Wagenaar et al., 2005): this promising solution (decrease of the excretion from 1 to 2 Log) will face the problem of a potential selection of a resistive mutant strain.

– Vaccination (de Zoete et al., 2007): Few developments are under way on this subject; the effectiveness of the vaccines remains currently hypothetical.

– Use of probiotics, prebiotics, and bacteriocins has been considered by nume- rous teams (Willis et Reid, 2008; Morishita et al., 1997) with sometimes convin- cing results.

(9)

– Supplementing the food with organic acids (Chemaly et al., 2007; Solis de los Santos et al., 2008 ) and particularly caprylic acid seems promising (3 to 4 Log decrease).

– Finally, the development of specific barrier flora (Laisney et al., 2004) could constitute a direction to be investigated.

All of these strategies require that they be proven on the field to ensure their effi- ciency.

Until then, the best prevention for flock contamination by Campylobacter remains the introduction of reinforced biosecurity measures (Refregier-Petton et al., 2001).

The decrease of Campylobacter carcass contamination at the slaughterhouse, in addition to the application of sanitary measures, includes early refrigeration in low hygrometric conditions. Because Campylobacter is sensitive to desiccation, it is possible to reduce carcass contamination levels from 0.5 to 0.8 Log by chilling it in 80% controlled hygrometric conditions (Salvat, unpublished results). Another method to reduce water activity on the carcass surface consists in freezing it which results in a decimal reduction of Campylobacter. This technique is being used by Denmark and Norway in their Campylobacter control plan (EFSA, 2007). Finally, one possible strategy, although currently forbidden in Europe, remains carcass decon- tamination (Salvat et al., 1997; Refrégier-Petton et al., 2003).

4 – CONCLUSION

The prophylaxis of Salmonella in animal chains is now well established (poultry chain) or soon will be (pork chain) and is based on firm epidemiologic information.

It is different in the case of Campylobacter, the physiology and epidemiology of which are currently less well known and for which control strategies will likely be less ambitious and will rely on different scientific and technical solutions, which will not aim at eradication but rather at the decrease of micro-organism propagation in the food chain.

REFERENCES

AFSSA, 2004. Appréciation des risques alimentaires liés aux Campylobacters : Application au couple poulet/Campylo- bacter jejuni. 96 p.

AFSSA. 2006. RAPPORT FINAL. Décembre 2006. Convention AFSSA/DGAl S 04/14.

71 p.

AFSSA. 2007. RAPPORT FINAL. Décembre 2007. Convention AFSSA-DGAL S 05/32.

62 p.

BRYNESTAD S., BRAUTE L., LUBER P., BAR- TELT E., 2008. Int. J. Risk Assessment and Management. 8(3), 194-213.

BELOEIL P.-A., FRAVALO P., FABLET C., JOLLY J.-P., EVENO E., HASCOET Y., CHAUVIN C., SALVAT G., MADEC F., 2004. Prev. Vet. Med. 63(1-2), 103-120.

BELOEIL P.A., CHAUVIN C., PROUX K., FABLET C., MADEC F., ALIOUM A., 2007.

Vet. Research. 38(6), 835-848.

(10)

DENIS M., CHIDAINE B., LAISNEY M.-J., KEMPF I., RIVOAL K., MÉGRAUD F., FRAVALO P., 2008. Path. Biol. In press.

DE ZOETE, M.R. VAN PUTTEN, J.P.M.

WAGENAAR, J.A. 2007. Vaccine. 25(30 spec. Issue), 5548-5557.

CHEMALY M., LALANDE F., QUÉGUINER M., FRAVALO P., 2007. CHRO. V 54, supple- ment 1, p. 139.

EFSA. 2004. The EFSA Journal (2004) 177 1- 10

EFSA, 2007. The EFSA Journal (2007) 98, 1- 85.

EFSA, 2007. The EFSA Journal 2007 – 351.

EFSA, 2007. The EFSA Journal (2007) 97.

EFSA, 2008. The EFSA Journal (2008) 135, 1- 111.

EFSA. 2008. The EFSA Journal (2008) 134, 1- 91

EU, 2003. DIRECTIVE 2003/99/EC OF THE EUROPEAN PARLIAMENT AND OF THE COUNCIL of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council decision 90/

424/EEC and repealing Council Directive 92/117/EEC. Official Journal of the Euro- pean Union. 12/12/2003.

EU, 2003. REGULATION (EC) No 2160/2003 OF THE EUROPEAN PARLIAMENT AND OF THE COUNCIL of 17 November 2003 on the control of salmonella and other specified food-borne zoonotic agents.

Official Journal of the European Union. 12/

12/2003.

EU, 2005. COMMISSION REGULATION (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Offi- cial Journal of the European Union. 22/12/

2005.

FRAVALO P., LAISNEY M.J., GILLARD M O, SALVAT G., CHEMALY M., 2008, Soumis au J. Food Protect. (available from the author)

GALLAY, A. BOUSQUET, V. SIRET, V. PROU- ZET-MAULÉON, V. DE VALK, H.

VAILLANT, V. SIMON, F. LE STRAT, Y.

MÉGRAUD, F. DESENCLOS, J.-C. 2008.

J. infect. Diseases. 197(10), 1477-1484.

GILLESPIE I.A., OBRIEN S.J., NEAL K.R., FROST J.A., COWDEN J.M., SYED Q., 2005. J. Infection. 50(3). 265-267.

InVS, juin 2003. Morbidité et mortalité d’origine alimentaire, tome I . Produced in col- laboration with AFSSA

LAISNEY M.J., GILLARD M.O., Salvat G., 2004. British Poult. Sci. 45(1), 49-54.

LINDQVIST R., LINDBLAD M., 2008. Int. J.

Food Microb. 121(1), 41-52.

LUBER P., BRYNESTAD S., TOPSCH D., SCHERER K., BARTELT E., 2006. Appl.

Env. Microb. 72(1), 66-70.

MORISHITA T.Y., AYE P.P., HARR B.S., COBB C.W., CLIFFORD J.R., 1997. Avian Diseases. 41(4), 850-855.

PAYOT S., DRIDI S., LAROCHE M., FEDERI- GHI M., MAGRAS C., 2004. Vet. Microb.

101(2), 91-99.

POIRIER E., WATIER L., ESPIÉ E., WEILL F.X., DEVALK H., DESENCLOS J.C., 2008. Epi- dem. Infect. 136(9) 1217-1224.

RÉFRÉGIER-PETTON J., ROSE N., DENIS M., SALVAT G., 2001 Prev. Vet. Med. 50(1-2), 89-100.

REFRÉGIER-PETTON J., KEMP G.K., NEBOUT J.M., ALLO J.C., SALVAT G., 2003. Brit. Poult. Sci. 44(5), 790-791.

ROSENQVIST H., NIELSEN N.L., SOMMER H.M., NORRUNG B., CHRISTENSEN B.B., 2003. Int. J. Food Microb. 83(1), 87- 103.

SOLIS DE LOS SANTOS F., DONOGHUE A.M., VENKITANARAYANAN K., REYES- HERRERA I., METCALF J.H., DIRAIN M.L., AGUIAR V.F., BLORE P.J., DONO- GHUE D.J., 2008. Applied Env. Microb.

74(14), 4564-4566.

VAILLANT V., DEVALK H., BARON E., ANCELLE T., COLIN P., DELMAS M.C., DUFOUR B., POUILLOT R.,LE STRAT Y., WEINBRECK P., JOUGLA E., DESEN- CLOS J.C. 2005. Foodboren Path.

Disease. 2(3), 221 232.

WAGENAAR J.A., VANBERGEN M.A.P., MUELLER M.A., WASSENAAR T.M., CARLTON R.A., 2005. Vet. Microbiol.

109(3-4), 275-283.

WEHEBRINK T., KEMPER N., BEILAGE E.G., KRIETER J., 2008. Berliner and Munche- ner Tierart. Woch. 121(1-2), 27-32.

WILLIS W.L., REID L., 2008. Poultry Sci. 87(4), 606-611.