Qualitative and quantitative risk assessment for human salmonellosis due to multi-resistant Salmonella Typhimurium DT104 from consumption of Danish dry-cured pork sausages

Qualitative and quantitative risk assessment for human salmonellosis due to multi-resistant Salmonella Typhimurium DT104 from consumption of Danish dry-cured pork sausages
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  Qualitative and quantitative risk assessment forhuman salmonellosis due to multi-resistant Salmonella  Typhimurium DT104 fromconsumption of Danish dry-curedpork sausages Lis Alban a,* , Anne-Mette Olsen a , Bent Nielsen a ,Rie Sørensen b , Birthe Jessen b a  Danish Bacon and Meat Council, The National Committee for Pig Production, Axelborg, Axeltorv 3, DK-1609 Copenhagen V, Denmark  b  Danish Meat Research Institute, Maglega˚ rdsvej 2, DK-4000 Roskilde, Denmark  Received 5 April 2001; accepted 16 September 2001 Abstract Salmonella  Typhimurium DT104 (DT104) is unwanted in products for human consumption dueto its antibiotic resistance and ability to cause disease. We intended to set up an improvedmonitoring and management program to aid in deciding when to use pork contaminated withDT104 for production of sausages without jeopardizing consumer safety. We started by carrying outtwo assessments of the risk for human health associated with consumption of sausages produced by:(1) Danish pork from average slaughter days; (2) imported pork (IMP) with average prevalence of DT104. The assessments showed that, if   Salmonella  is present, it is usually in lower numbers(  50 per 400 cm 2 surface). Additionally, during processing, the numbers will be reduced by at least2 log-units. In Danish (DK) pork, DT104 constitutes 0.2–1.0% of the  Salmonella  isolates reported,while in imported pork (IMP), 18%. We estimated that out of one million, 25 g servings of DK dry-cured sausages, up to two DT104 bacteria could be found in each of 245 servings. Out of onemillion servings of 25 g IMP dry-cured sausages, up to two DT104 bacteria would occur in each of 19,260 servings. # 2002 Elsevier Science B.V. All rights reserved. Keywords:  Risk assessment;  Salmonella  Typhimurium DT104; Meat; Sausages; Processing; Monte CarlosimulationPreventive Veterinary Medicine 52 (2002) 251–265 * Corresponding author. Tel.:  þ 45-33-73-26-93; fax:  þ 45-33-14-57-56. E-mail address : (L. Alban).0167-5877/02/$ – see front matter # 2002 Elsevier Science B.V. All rights reserved.PII: S0167-5877(01)00258-6  1. Introduction Salmonella  Typhimurium DT104 (DT104) is typically a multi-resistant strain of   Sal-monella , and is unwanted in ready-to-eat products because of the risk for human health.In1996,DT104wasisolatedforthefirsttimeinDanishlivestock.Between1996and2000,95swine or cattle herds were found positive for DT104 (Anon., 2000a). Recently, DT104 wasalso observed in Danish poultry ( Despitedepopulation of affected swineherds, it has not been possible to stop the disseminationof the bacteria. It is assumed that DT104 nowadays is sub-clinically present in a consider-able proportion of Danish animals, and that eradication is impossible (Anon., 2000a).Therefore,theDanishDT104policyiscurrentlyunderreconsiderationtooptimiseresourceallocation without jeopardising consumer safety (Anon., 2000a). Additionally, importedpork can contain DT104 in larger amounts, because only the Scandinavian countries havenational surveillance strategies to decrease the prevalence of   Salmonella .According to current Danish law, meat with DT104 (assumed prevalence  0.01%) hasto be heat treated but in case of sporadic findings of DT104 (assumed prevalence <0.01%),themeatmaygodirectlytotheconsumer(Anon.,2000a).However,nomonitoringisabletoidentify all meat contaminated with DT104. Therefore, we were interested in setting up ageneral monitoring and management program which would include an indication whenpork could be used for sausage production as a way to deal with DT104. To get a scientificbasisforthis,weassessedwhetherdry-curedsausagesproducedbyporkwithDT104 could jeopardise consumer safety. One assessment was made for dry-cured sausages producedusing Danish pork and one was made for sausages produced using imported pork. 2. Material and methods Theguidelines forconducting riskassessmentdescribed byCodexAlimentarius(Anon.,1999) were followed as closely as possible. However, data were not available for all items(e.g. dose-response for development of disease when consuming DT104). Initially, aqualitative risk assessment was carried out; and next, a quantitative risk assessmentmodelling the prevalence of DT104 in servings of dry-cured sausages (as data of sufficientquality were available). 2.1. Hazard identificationS.  Typhimurium is unwanted in foods because it causes disease in man. The phage typeDT104 is even more unwanted because of its antibiotic resistance (potentially aggravatingthe course of disease in people).DT104 was observed for the first time in 1984 in the UK (Threlfall et al., 1996). AnEnglish study showed that DT104 caused a more-severe disease than usually observed ininfections with  S.  Typhimurium (Wall et al., 1994). Other studies from the USA and UK have not been able to confirm this (Davies et al., 1996; Hosek et al., 1997). DT104 doesnot seem to be more invasive than other types of   S.  Typhimurium (ILSI, 2000). Most Salmonella  infections are self-limiting, and according to The National Central Laboratory 252  L. Alban et al./Preventive Veterinary Medicine 52 (2002) 251  –  265  of the Danish Health System, treatment failures due to the antibiotic resistance have notbeen noticed. Reduced treatment ef  fi cacy can be expected in the cases of mono-therapywith, e.g. ampicillin, or if the bacteria have reduced sensitivity to quinolones, aminoglyco-sides, or cephalosporines (Anon., 2000a).In Denmark,  S.  Enteritidis was the most common cause of salmonellosis in 1999. Thesecond most common cause was  S.  Typhimurium, of which one-quarter was DT104. In1999, 3268 cases of human salmonellosis were reported, and perhaps 300 of these wererelated to pork (Anon., 2000b). During the years 1997 – 1999, a relatively constant number(around 40 per year) of sporadic cases of human DT104 with unknown cause have beenreported. Some of these cases may have been caused by imported food, in particular, pork and poultry products (Anon., 2000a). Apart from the sporadic cases, three minor outbreakshave been observed: one related to a private slaughterhouse (M ø lbak et al., 1999), thesecond to a restaurant (cross-contamination most likely with imported pork), and the thirdto a butcher (isolated from roast beef) (Anon., 2000b). 2.2. Exposure assessment  Risk factors for acquiring DT104 include consumption of contaminated food likepoultry, pork, and beef, as well as contact with diseased production animals and pets(Wall et al., 1994; Davies et al., 1996). In the present assessment, we focused on pork andexcluded the live pig. We looked on the prevalence of   Salmonella  and speci fi cally DT104,as well as the possibility of growth in pork and dry-cured sausages. Cross-contaminationoccurring at the consumer level was not addressed. 2.2.1. Prevalence in pork  Since 1995, Denmark has conducted a national  Salmonella  surveillance and controlprograminswineherdsproducing>100 fi nishersperyear.Basically,itconsistsofstrategieswithinfeedmills,breedingandmultiplierherds,piglet-producingherds,and fi nisherherds.Finisher herds are surveyed serologically. Every month,  fi nisher herds are assigned to oneof three levels according to the seroprevalence during the previous 3 months (Mousinget al., 1997). Among approximately 16,000  fi nisher herds surveyed in Denmark in 1999,1368 herds had an increasedantibody seroprevalence level.These herds subsequently wereenrolled in a bacteriologic follow-up, and DT104 was identi fi ed in 11 of the 1368 herds(Anon., 2000b). However, in year 2000, DT104 was found in 43 herds (Anon., 2001).Since, 1 January 1998, approximately 25,000 samples of Danish pork have beenanalysed yearly in the national surveillance of fresh pork. Additionally, 37,000 pooledexport samples (each pool consists of   fi ve samples) have been examined per year. Salmonella  was isolated in approximately 1% of the samples (Anon., 2000b), andDT104 in 0.002% of the samples. If each of these positive pooled samples consisted of not just one but  fi ve positive samples, a maximum observed prevalence of DT104 wouldhave been 0.01% (Olsen, 2001, pers. commun.). Data from two other projects — with anover-representation of herds with higher prevalence of   Salmonella  (S ø rensen et al., 2000;Olsen, 2001) — demonstrate that when  Salmonella  is present, most commonly it is in lowernumbers (  50 per 400 cm 2 surface) (Table 1). Finally, none of 3500 carcases fromslaughter days in which a known DT104 herd delivered  fi nishers was positive for DT104.  L. Alban et al./Preventive Veterinary Medicine 52 (2002) 251  –  265  253  In July 1998, surveillance was initiated for DT104 in imported fresh or frozen pork (Anon., 1998). Up to the end of 1999, 1104 samples have been tested; 7.7% were positivefor  Salmonella , and 1.4% for DT104 ( (18% of the  Salmonella  isolates). Preliminary data for year 2000 are in line with the previous data: Salmonella was present in 140 out of 629 (21%) examined batches, and DT104 in 20 (3%).Inconclusion,DT104 seldom isfoundinDanish fi nisher herds; however,latelytherehasbeen an increase in the prevalence. There is a sporadic prevalence of DT104 in Danishpork, whereas imported pork  — compared to Danish pork  — has a higher prevalence of  Salmonella  (and speci fi cally of DT104) so far. When DT104 is present, it is usually inlower numbers (  50/400 cm 2 ) (Table 2), evenon carcasses srcinating from herds with thehighest  Salmonella  seroprevalence. This is expected to be the case for imported pork, too. 2.2.2. Possibilities of growth in pork  Inadequate cooling as well as storage and transportation of pork at temperatures >7  8 Ccan cause growth of   Salmonella  (ICMSF, 1998). 2.2.3. Prevalence in dry-cured sausages Danish dry-cured sausages are produced with starter culture (bacteria) or glucono- d -lacton (GdL) (chemical) to control the pH decline. The process is initiated at a tempera-ture of 20 – 24  8 C and 90 – 95% relative humidity. At the end of processing, most of theproducts contain 10 – 14% salt in water, and usually, 20 – 25% of the weight is reduced bydrying. Final pH is approximately 4.8 – 5.0. Because, no heat treatment is involved in theproduction, there is a risk that  Salmonella  might be present in the  fi nal product.During 1998 – 2000, the Danish authorities have surveyed retail outlets and analysed960 samples of pork sausages either in their routine surveillance or screening;  Salmonella Table 1Input data and derived quantitative distributions of   Salmonella  on a piece of Danish and imported pork,respectively, for year 2001, for use in simulation of number of DT104 in dry-cured sausagesNo. of   Salmonella bacteria Salmonella  prevalence (%)Input data: distribution of positive samples Derived distributions on a250 g piece of meat andfat for sausage production from1 g of caecalcontentSwabs of 400 cm 2 outer surfaceConservativeaveragedistributionDenmark Other countries(imported)0 0 0 0.0 98.333 92.185 52 58 50.0 0.833 3.9150 11 18 17.0 0.283 1.33500 12 24 a 17.0 0.283 1.335000 25 b 24 a 10.5 0.175 0.8250000 25 b 24 a 5.5 0.092 0.43 a Only two dilutions were analysed; the highest titres were >50 (Olsen et al., 2000). b Only three dilutions were analysed; the highest titres were >500 (S ø rensen et al., 2000).254  L. Alban et al./Preventive Veterinary Medicine 52 (2002) 251  –  265  Table 2Description of input data used for simulating the number of DT104 in Danish dry-cured sausagesVariable Input data Derived distribution Origin of informationPrevalence of   Salmonella in Danish pork 1.0%: all pork; 1.6%: sausage pork;5105 samples analysed: 83  Salmonella -positive slaughterhouse variationPert distribution: minimum  ¼  0.0%;mode  ¼  0.5%; maximum  ¼  8.0%Routine surveillance data from theDanish slaughterhousesPrevalence of   Salmonella in imported pork 1104 samples analysed: 85 Salmonella -positiveBeta distribution: r  ¼ 85 ; n ¼ 1104 ;  p ¼ 7 : 7 % Import control data, please of sausage production Usually: many small pieces of pork primarily from the fore-endFixed distributions 960 piecesof 250 gExpert opinion from establishmentsproducing sausagesPathogen reduction associatedwith sausage productionminimum  ¼  1.8 log-units;maximum  ¼  5.3 log-unitsPert distribution: minimum ¼ 2 : 0log-units; mode ¼ 2 : 2 log-units;maximum ¼ 3 : 0 log-unitsData from pilot experimentsRelative distribution of DT104compared to  Salmonella 0.2 – 1.0%, Danish pork; 18.0%,imported pork Fixed distributions: 1%, Danish;18%, importedRoutine surveillance data from theDanish slaughterhouses and importcontrol dataServing sizes (g) Child: 10; adult: 25; party: 40 Expert opinionPrevalence of   Salmonella  in sausages(used for validation of model results)1618 negative samples in manufacturers ’  own check programme; 300negative samples from sausage production with DT104 pork; positive sampleshave been found in a retail outlet only once, and here, cross-contaminationcould not be ruled out (960 samples were analysed)Routine surveillance data from theDanish slaughterhouses and retail outlets L  .A  l    b  a n e t   a l    . /   P r  e v  e n t   i   v  e V  e t   er  i   n ar   yM e d  i   c i   n e 5 2  (  2  0  0 2  )  2  5 1  – 2  6  5  2   5   5  
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