Surveillance and outbreak reports

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1 Surveillnce nd outrek reports Epidemiologicl nd microiologicl investigtion of lrge outrek of monophsic Slmonell Typhimurium 4,5,12:i:- in schools ssocited with imported eef in Poitiers, Frnce, Octoer 2010 M E Rguenud (mrie-eve.rguenud@rs.snte.fr) 1, S Le Hello 2, S Slh 3, F X Weill 2, A Brisois 4, G Delms 5, P Germonneu 1 1. French Institute for pulic helth surveillnce, Poitiers regionl office, Frnce 2. Institut Psteur, Ntionl Reference Centre for Slmonell, Pris, Frnce 3. Direction générle de l limenttion (DGAL), Pris, Frnce 4. Lortory for Food Sfety (ANSES), Pris, Frnce 5. French Institute for pulic helth surveillnce (InVS), Deprtment of infectious diseses, Frnce Cittion style for this rticle: Rguenud ME, Le Hello S, Slh S, Weill FX, Brisois A, Delms G, Germonneu P. Epidemiologicl nd microiologicl investigtion of lrge outrek of monophsic Slmonell Typhimurium 4,5,12:i:- in schools ssocited with imported eef in Poitiers, Frnce, Octoer Euro Surveill. 2012;17(40):pii= Aville online: Article sumitted on 16 Mrch 2012 /pulished on 4 Octoer 2012 An outrek due to the emerging monophsic Slmonell Typhimurium 4,5,12:i:- occurred in four schools in Poitiers in Octoer Food trce-ck investigtion led to the identifiction of eef urgers s the cuse of the outrek nd their susequent withdrwl. The Institute for Pulic Helth Surveillnce conducted retrospective epidemiologicl investigtion to ssess the extent of the outrek nd descrie cses. Self-dministered questionnires were completed y students nd personnel ttending ech of the four schools ffected. Clinicl cses were defined s nyone hving eten t the school when the eef urgers were served nd reporting dirrhoe or fever with t lest one digestive symptom (nuse, vomiting or dominl pin), within five dys fter the incriminted school mel or with unknown dte of onset within 15-dy period fter the incriminted school mel. Of 1,559 persons exposed, 554 clinicl cses were identified corresponding to n overll ttck rte of 35.5%. Of 554 clinicl cses, totl of 286 (53%) sought medicl cre nd 31 (6%) were hospitlised for more thn 24 hours. This multi-school outrek is one of the iggest food-orne outreks of monophsic Slmonell Typhimurium 4,5,12:i:- descried in Frnce. Prompt notifiction of cses nd rpid identifiction nd withdrwl of the incriminted tch of eef urgers ws crucil to limit the extension of this outrek. Introduction In Frnce, during the period , Slmonell ws the cuse of 23% of dispersed food-orne outreks [1]. Monophsic Slmonell Typhimurium 4,5,12:i:-, n emerging vrint of serotype Typhimurium, is responsile for n incresing numer of food-orne outreks in Europe [2-4]. The prevlence of this serotype mong humn slmonellosis cses hs incresed considerly since the mid-1990s. In the first decde of the 2000s, this serotype represented one of the most common serotypes mong humn cses in mny countries round the world [5-8]. In Frnce, the incidence of serotype 4,5,12:i:- incresed in the pst decde nd hs ecome the third most common serotype identified in humns since 2008 [9]. In 2010 nd 2011, the suspecies enteric serotype 4,5,12:i:- ws identified in two ntionwide outreks in Frnce linked to dried pork susge [2,10]. Dt on the severity of clinicl illness for those infected with serotype 4,5,12:i:- re still limited nd reported hospitlistion rtes vry mong studies [4,11]. In Octoer 2010, the regionl helth gency, the locl Food Control Unit nd the regionl office of the Institute for Pulic Helth Surveillnce investigted food-orne outrek involving out 50 known cses ttending four schools of Poitiers. The first eight cses were notified during school holidys. Monophsic Slmonell Typhimurium 4,5,12:i:- ws isolted from stool smples of these first cses. Investigtions y the Food Control Unit quickly identified frozen eef urgers produced in nother Europen Union (EU) Memer Stte s the cuse of the outrek. The met originted from single tch tht ws served for lunch in the first two schools reporting cses. Two dys fter notifiction of the first cses nd without witing microiologicl results on the products, the ntionl food sfety uthorities (DGAL) sked the distriutor to stop ll deliveries to its clients (schools nd resturnts). Four dys lter, DGAL initited the withdrwl of ll frozen eef urgers tches (22 tches in totl) with the sme production dte s the incriminted tch. As the Slmonell serotype identified is n emerging one in Frnce nd in Europe, the regionl helth 1

2 Tle 1 Study prticiption y school, Slmonell outrek, Poitiers, Frnce, Octoer 2010 School Persons in the school (including personnel) n Questionnires received nd prticiption rte in schools n (%) Prticipnts exposed to mel n Mels distriuted n Prticiption rte of persons exposed to mel A (92) >100 B (91) C (76) D (46) Totl 2,723 2,131 (78) 1,559 1, Persons who te lunch on 22 Octoer t Schools B, C, D nd on 19 Octoer t School A. More prticipnts thn mels served. % uthorities nd the Institute for Pulic Helth Surveillnce decided to conduct n in-depth nlysis of the outrek nd to mesure its extent. This rticle descries the epidemiologicl nd microiologicl investigtions undertken to estimte the totl numer of cses involved in the outrek of monophsic Slmonell Typhimurium 4,5,12:i:- in the schools of Poitiers nd to descrie their chrcteristics. Methods Epidemiologicl investigtion Twelve dys fter the initil lert, the regionl office of the Institute for Pulic Helth Surveillnce conducted retrospective epidemiologicl investigtion in the four schools of Poitiers where the incriminted tch of frozen eef urgers hd een served nd where t lest one cse of gstrointestinl disese ws reported. We otined the weekly menus of food served t the schools directly from the kitchen supervisors in order to know t which dy(s) the incriminted eef ws served nd to hve confirmtion tht there ws only one single type of mel served per dy. A self-dministered questionnire ws distriuted to ll students nd personnel of the four schools. The questionnire focused on consumption of school mel on the dy(s) the incriminted eef ws served, ge nd sex, timing of illness, clinicl symptoms nd tretment. As the questionnire ws sent nerly two weeks fter the dte the incriminted eef ws served, we sked persons interviewed out the dte they te lunch t school insted of sking them out specific food items. A clinicl cse ws defined s person hving eten the school mel on the dy the incriminted eef ws served nd reporting either: (i) dirrhoe within five dys fter school mel, or (ii) fever with t lest one digestive symptom (nuse, vomiting or dominl pin) within five dys fter school mel, or (iii) dirrhoe of unknown dte of onset ut within 15 dys fter the incriminted school mel, or (iv) fever with t lest one digestive symptom nd with unknown dte of symptoms within 15 dys fter the school mel. Confirmed cses were clinicl cses with positive stool culture for monophsic Slmonell Typhimurium 4,5,12:i:- s determined y the French Ntionl Reference Centre for Slmonell (NRC). In order to clculte the prticiption rte, the numer of mels delivered on the dy(s) the contminted eef ws served ws used s proxy vlue for the numer of individuls exposed to the incriminted mel. Only individuls who reported hving eten the school lunch on the dy the incriminted eef ws served were considered to e exposed. We ssume tht ll those who te t the school consumed the eef s only one type of mel is served for lunch on given dy. Attck rtes for disese nd their 95% confidence intervls (CI) were clculted y ge, sex, nd school. Sttisticl nlyses were conducted in STATA 10 (SttCorp, Tx). This investigtion ws conducted with the uthoristion of the French regultory uthority (Commission ntionle de l informtique et des liertés, request numer relted to outrek investigtion). Microiologicl investigtions The Food Control Unit collected frozen eef urger from one school nd cooked eef urger from smple mel from second school. Concentrtion of cteril inoculum ws mesured y the Lortory for Food Sfety (ANSES). Twenty-five humn Slmonell isoltes collected etween 25 nd 31 Octoer 2010 y the lortories of Poitiers nd the two food isoltes were sent to the NRC in Pris for serotyping, sutyping nd 2

3 Tle 2 Chrcteristics of the exposed popultion, Slmonell outrek, Poitiers, Frnce, Octoer 2010 (n=1,559) School A B C D Sex-rtio (mle/femle) Adults ( 20 yers-old) Numer of exposed Numer of clinicl cses Adolescents (<20 yers-old) Numer of exposed Numer of clinicl cses Medin ge in yers (interqurtile rnge) Adults ( 20 yers-old) 43 (38 53) 40 (34 51) 41 (28 45) 39.5 (29 51) Adolescents (<20 yers-old) 13 (11 13) 12 (11 13) 12 (11 13) 16 (15 17) As 21 questionnires missed informtion on sex, 1,538 questionnires were used, For cses whose ge ws known. As 20 questionnires missed informtion on ge, 1,539 questionnires were used. ntimicroiologicl susceptiility nlysis. Sutyping of the isoltes ws crried out y stndrdised XIpulsed-field gel electrophoresis (PFGE) nd y multilocus vrile-numer tndem repet nlysis (MLVA), s previously descried [2,12]. The MLVA profiles were expressed ccording to the nomenclture pulished y Lrsson et l [13]. The ntimicroil susceptiility testing to 32 ntimicroils ws performed y disk diffusion on Mueller-Hinton gr ccording to the guidelines of the Antiiogrm Committee of the French Society for Microiology. Humn isoltes were compred with isoltes from food using the sme typing methods. Results Epidemiologicl results From the 2,723 questionnires distriuted, 2,139 questionnires were received (78.5%), from which eight were excluded from nlysis ecuse school informtion ws missing. A totl of 1,559 prticipnts declred hving eten t school on the dys the incriminted eef urgers were served. Bsed on numer of mels distriuted on the dy(s) the incriminted eef urgers were served (n=1,806), this represented study prticiption rte of 86% cross ll schools for persons exposed (Tle 1). Three schools (Schools A, B nd C) were Junior high schools (with 4 different levels) nd one school (School D) ws Senior high school (3 higher levels). Medin ge of dolescents (<20 yers-old) ttending the school ws higher in School D (medin ge of 16 yers, rnge 14 19) thn in the other schools (medin ge of yers, rnge 10 16). All schools were mixed (Tle 2). The sex-rtio of study prticipnts ws 1.0. School D hd mjority of mle students (sex-rtio: 2.3) (Tle 2). Exposed dults ( 20 yers-old) represented 11of 265 (4%) of ll exposed in School A, 33 of 704 (5%) in School B, nd seven of 440 (2%) in School C (Tle 2), nd were minly personnel of the school. Adults in School D represented 14 of 130 exposed (11%) nd included oth personnel nd students. The epidemic curve of clinicl cses per school is shown in the Figure. Only cses who reported the dte of onset of their illness re included (n=493). The pek of the outrek in School A occurred two dys fter the incriminted lunch ws first served. At this school, the incriminted eef urgers were served on 19 Octoer, nd 25 dditionl eef urgers were lso served on the following dy. The pek of the outrek in Schools B nd D occurred one dy fter the incriminted lunch ws served, nd in School C, two dys fter. In the three lter schools, the incriminted lunch ws served on 22 Octoer. Among the 1,559 persons exposed, 554 were identified s clinicl cses: 493 presented symptoms within five dys fter the lunch nd 61 presented symptoms with n unknown time of onset within two weeks fter the lunch. The glol ttck rte ws 35.5% (554/1,559). Attck rtes were similr mong persons of femle nd mle sex (Tle 3) (proportion test; p=0.46). Attck rte ws significntly higher (proportion test, p<0.001) mong dolescents (<20 yers-old) (534/1,474, 36%) compred to dults (10/65, 15%) lthough rtes 3

4 Figure Clinicl cses y dte of symptom onset nd school, Slmonell outrek in schools, Poitiers, Frnce, Octoer 2010 (n=493) School A School B School C School D 120 Numer of clinicl cses Beef urgers served t School A Additionl eef urgers served t School A (n=25) Beef urgers served t Schools B, C, D Food-orne outrek lert y Poitiers university hospitl /10/ /10/ /10/ /10/ /10/ /10/ /10/ /10/ /10/2010 Dte of symptom onset vried mong schools (Tle 3). The risk of developing symptoms of gstroenteritis fter eting the incriminted lunch ws 2.3 times greter for dolescents compred to dults (95% CI: ). Within the dolescent ge group, the risk of developing symptoms of gstroenteritis decresed significntly with incresing ge (chi-squred test for liner trend=40.2, p<0.001). Attck rtes clculted per school re shown in Tle 3. The highest ttck rte ws found for School B (46.8%). Attck rte ws significntly lower for School C (17%) thn for ech of the other schools (proportion test, p<0.001). The risk of developing symptoms of gstroenteritis fter eting lunch t one of the three Schools A, B nd D ws 1.78 times higher thn for School C (95% CI: ). The risk of developing symptoms of gstroenteritis fter eting lunch t School B ws 2.76 times higher thn tht for School C (95% CI: ). Among the 554 clinicl cses, the three most frequently reported clinicl symptoms were dirrhoe (490 cses, 88%), dominl pin (451 cses, 81%) nd fever (389 cses, 70%) (Tle 4). Other reported symptoms included nuse (250 cses, 45%) nd vomiting (179 cses, 32%). Tle 4 descries the frequency of symptoms in cses per school. More thn hlf of cses (53 %) reported hving consulted doctor in privte prctice or in hospitl setting. A totl of 31 cses (6%) reported hving een hospitlised for t lest 24 hours (Tle 4). Medin hospitl sty clculted for 27 of the 31 hospitlised cses ws three dys (95% CI: 1 4). A totl of 41 cses (7%) declred hving stool culture positive for Slmonell (n=33) or hving positive result (test not specified) (n=8). The medin incution time clculted for the 296 cses who reported the time of onset of their symptoms in ddition to the dte of onset ws 40 hours (95% CI: 27 56) (Tle 4). The first cse occurred one hour fter lunch nd the lst cse 127 hours fter lunch. Medin incution ws shortest (34 hours) for cses ttending School B nd longest (49 hours) for cses ttending School A. Among the 1,005 persons who hd lunch the dy the incriminted eef urger ws served ut who did not fit the cse definition, 52 reported gstrointestinl symptoms eginning more thn five dys fter the lunch (rnge: 6 34 dys). Of these, 34 reported hving 4

5 Tle 3 Attck rte per ge group, sex nd school, Slmonell outrek, Poitiers, Frnce, Octoer 2010 (n=554) Cses / exposed Attck rte % (95% confidence intervl) Age group Adolescents (< 20 yers-old) 534 / 1, (33,8 38,7) Adults ( 20 yers-old) 10 / (7,6 26,5) Sex Femle 261 / (31,3 38,2) Mle 287 / (33,1 40,0) School A 95 / (29,7 41,5) B 333 / (43,0 50,5) C 76 / (13,6 20,7) D c 50 / (30,1 47,4) All schools 554 / 1, (33,1 38,0) For persons with ville informtion. Junior high school (medin ge of students: 16 yers). c Senior high school (medin ge of students: yers). dirrhoe only nd 18 reported fever with t lest one digestive symptom. Microiologicl results The two food isoltes from frozen nd from cooked eef urger smpled in the cnteen of Schools A nd B were monophsic Slmonell Typhimurium 4,5,12:i:- with resistnce to mpicillin, streptomycin, sulphonmides nd tetrcycline (R(resistnt)-type ASSuT), which is common to this strin [9]. Concentrtion of cteril inoculum ws 270 to 18,000 (colony-forming unit) CFU/g for the 23 enumertions crried out. The NRC confirmed the presence of monophsic Slmonell Typhimurium 4,5,12:i:- (R-type ASSuT) in the 25 humn isoltes. Among these, 21 elonged to students who stisfied the cse definition used in the study, three elonged to students who were ill ut who did not stisfy the cse definition used in the study (one with fever only nd two with time of onset t nine nd 10 dys fter the incriminted lunch) nd one elonged to student who did not prticipte in the questionnire survey. Food nd humn isoltes exhiited unique PFGE profile (XTYM-151) nd unique MLVA profile ( NA-211). Discussion nd conclusion A locl school outrek of monophsic Slmonell Typhimurium 4,5,12:i:- cused y imported food ws identified through the ntionl disese notifiction system for food-orne illness. Investigtion y the Food Control Unit quickly identified the cuse of the outrek s eef urgers nd ll tches of the sme dte thn the incriminted tch were rpidly withdrwn. The impct of the consumption of the incriminted eef urgers ws unknown t the time of outrek notifiction s it occurred during school vction. The retrospective epidemiologicl investigtion conducted in the four ffected schools of Poitiers enled us to identify 554 clinicl cses mong the 1,559 study prticipnts who te t school on the dys the incriminted eef urgers were served. Twenty-one cses who prticipted in the study were iologiclly confirmed y the NRC y serotyping. This multi-school outrek is one of the iggest food-orne outreks due to monophsic Slmonell Typhimurium 4,5,12:i:- descried in Frnce. A previously descried lrge outrek of Slmonell enteric serotype 4,[5],12:i:- in Frnce involved 337 identified cses nd occurred ntionwide etween 31 Octoer nd 18 Decemer 2011 [10]. Another ntionwide epidemic involving the sme Slmonell strin occurred in Frnce etween 1 August nd 9 Octoer 2011 with 682 cses reported [10]. In these two outreks, the investigtions indicted dried pork susge s eing the most likely source of the outreks [10]. The Poitiers school outrek is the first lrge scle outrek descried in Frnce of monophsic Slmonell enteric vrints involving eef. The overll ttck rte of the Poitiers outrek ws higher thn the verge ttck rte (7%) oserved in Slmonell food-orne outreks tht occurred in school cnteens in in Frnce [1]. In the sme period, no lrge-scle Slmonell outrek ws descried in school setting. The lrgest food outrek descried in schools in Frnce occurred in 2008 nd involved 1,137 identified cses with glol ttck rte of 50% nd ws of virl origin [14]. Although the Poitiers outrek occurred two months efore the nnul winter pek of virl gstroenteritis, we cnnot exclude tht some of the cses identified in the survey were due to other gstrointestinl disese. The high ttck rte oserved in this outrek could e explined y prticulrly high initil concentrtion of cteril inoculum. A met-nlysis y Teunis et l. [15] on food-orne outrek dt showed medin infective dose (ID50) vlues rnging etween 30 nd 50 CFU/g for Slmonell. The survey reveled n ttck rte twice s high mong dolescents s mong dults. Moreover, the ttck rte decresed with incresing ge mong dolescents. There re no ovious explntions for this finding other thn the possiility tht the younger students were served lunch t different time thn the others nd therey te eef with potentilly different cooking time. 5

6 Tle 4 Chrcteristics of clinicl cses with symptoms of gstroenteritis, Slmonell outrek, Poitiers, Frnce, Octoer 2010 (n=554) School A Medin incution time in hours, 49,43 69 IQR (numer of cses) (n=41) School B 34, 25 5 (n=204) School C 46, (n=22) School D 39, (n=29) All schools 40, (n=296) Clinicl symptoms 95 (100) 333 (100) 76 (100) 50 (100) 554 (100) Nuse 56 (41) 164 (49) 30 (39) 17 (34) 250 (45) Vomiting 34 (36) 119 (36) 12 (16) 14 (28) 179 (32) Adominl pin 74 (78) 285 (86) 52 (68) 40 (80) 451 (81) Fever 72 (78) 254 (76) 40 (53) 23 (46) 389 (70) Dirrhoe 82 (86) 295 (89) 65 (86) 48 (96) 490 (88) Other symptoms 16 (17) 45 (14) 14 (18) 1 (2) 76 (14) Tretment 95 (100) 333 (100) 76 (100) 50 (100) 554 (100) Doctor consulttion 48 (51) 201 (62) 18 (76) 19 (62) 286 (53) Hospitlistion for t lest 24 hours 6 (6) 22 (7) 2 (3) 1 (2) 31 (6) Stool culture 16 (17) 51 (17) 7 (9) 4 (8) 78 (15) IQR: interqurtile rnge. Unless otherwise specified. For cses who reported the time of onset of their symptoms in ddition to the dte. The outrek showed signs of severity with out hlf of the cses who sought medicl cre in privte prctice or n emergency service, of which 31 of 554 (6%) were hospitlised for more thn 24 hours. Incution for Slmonell infection is known to rnge from six to 72 hours with longer incutions (up to 16 dys) documented [16]. Two students with positive stool culture nd n incution of nine nd 10 dys could e secondry cses contminted y person-toperson spred. We oserved tht medin incution ws shortest in the school with the highest ttck rte (School B). Such negtive correltion etween ttck rte nd incution hs een documented in previous outreks nd retrospective nlysis of humn outreks [17]. This highlights the possiility tht the infective dose ws greter in eef urgers served in School B thn in other schools, in prticulr School C. Moreover, hospitlistion rte used s proxy mesure for disese severity in this context ws 2.6 times greter mong cses ttending School B thn mong those ttending School C. However, the possiility tht frozen eef urgers were contminted t different concentrtions is unlikely ecuse eef urgers supplied to schools were ll from the sme tch. One hypothesis for different ttck rtes oserved etween schools reltes to different cooking prctices. Although the numer of cses identified y the investigtion is proly close to the rel numer of cses of slmonellosis due to ingestion of contminted eef urgers, the numer could e underestimted ecuse of non exhustive study prticiption (response rte 78%), ecuse of our ssumption tht ll those who te t the school consumed the eef, nd ecuse of errors in reporting disese onset for persons with clinicl symptoms. Inversely, importnt locl medi ttention efore the conduct of the investigtion could hve induced high prticiption rte of the ill student group nd n over declrtion of symptoms due to psychogenic-like effect. The two-week dely etween the first cses nd the questionnire survey (due to school vction) could hve led to recll is nd errors, especilly in dte reporting. The risk of error for exposure ws minimised y sking students out the dte they te lunch t school insted of sking them the specific food items they hd eten. At the country s deprtmentl level, two other loclised outreks of monophsic Slmonell Typhimurium 4,5,12:i:- occurred in Octoer 2010, one in retirement institution nd nother in recretion centre ssocited with the consumption of eef urgers from the incriminted tch (18 cses, unpulished dt). Interviewing t ech of the eighteen other institutions in the deprtment tht received frozen eef urgers with the sme production dte s the incriminted tch reveled tht none ws wre of cses of dirrhoe within their institution (s of 9 Novemer 2010). Although distriution of potentilly contminted frozen eef urgers ws widespred in Frnce, no increse in food-orne outreks ws detected through disese notifiction surveillnce nd no locl increse in the serotype 4,5,12:i:- ws detected y the NRC (s of 9 Novemer 2010). 6

7 The interntionl dimension of this outrek in Frnce is demonstrted y the fct tht the eef ws produced in n estlishment in nother EU Memer Stte. The Rpid Alert System for Food nd Feed (RASSF) ws used to inform uthorities of the mnufcturer country nd other EU countries likely to receive the products. Only French distriutor received ll the tches from this Memer Stte mnufcturer nd sold them. Furthermore, no food-orne outreks cused y the monophsic Slmonell Typhimurium 4,5,12:i:- were reported in Europe t the time of the outrek in Poitiers. Monophsic Slmonell Typhimurium 4,5,12:i:- ws ssocited with severe outrek, the lrgest Slmonell food-orne outrek descried in school setting in Frnce in recent yers. Quick identifiction nd withdrwl of incriminted food tch nd respect of sfe cooking prctices for eef urgers were likely crucil to limit extension of outrek. Informing other Europen countries ws necessry s the incriminted eef ws n imported food product. References 1. Delms G, Jourdn d Silv N, Pihier N, Weill F-X, Villnt V, de Vlk H. Les toxi-infections limentires collectives en Frnce entre 2006 et [Collective food-orne infections in Frnce etween 2006 nd 2008]. Bull Epidémiol Hed. 2010;31-32: French. 2. Bone A, Noel H, Le Hello S, Pihier N, Dnn C, Rguenud ME, et l. Ntionwide outrek of Slmonell enteric serotype 4,12:i:- infections in Frnce, linked to dried pork susge, Mrch-My Euro Surveill.2010;15(24):pii= Aville from: spx?articleid= Echeit MA, Aldueñ A, Cruchg S, User MA. Emergence nd spred of n typicl Slmonell enteric susp. enteric serotype 4,5,12:i: strin in Spin. J. Clin Microiol. 1999;37(10): Mossong J, Mrques P, Rgimeu C, Huerty-Kru P, Losch S, Meyer G, et l. Outreks of monophsic Slmonell enteric serovr 4,[5],12:i: in Luxemourg, Euro Surveill. 2007;12(6): pii=719. Aville from: eurosurveillnce.org/viewarticle.spx?articleid= Switt AI, Soyer Y, Wrnick LD, Wiedmnn M. Emergence, distriution, nd moleculr nd phenotypic chrcteristics of Slmonell enteric serotype 4,5,12:i:-. Foodorne Pthog Dis. 2009;6(4): Centers for Disese Control nd Prevention (CDC). Investigtion of Outrek of Humn Infections Cused y Slmonell I 4,[5],12:i:-. Atlnt: CDC. 29 Oct Aville from: Amvisit P, Boonywiwt W, Bngtrkulmont A. Chrcteriztion of Slmonell enteric serovr Typhimurium nd monophsic Slmonell serovr 1,4,[5],12:i:- isoltes in Thilnd. J Clin Microiol. 2005;43(6): Tvechio AT, Ghilrdi AC, Fernndes SA. Multiplex PCR identifiction of the typicl nd monophsic Slmonell enteric susp. enteric serotype 1,4,[5],12:i:- in São Pulo Stte, Brzil: frequency nd ntiiotic resistnce ptterns. Rev. Inst Med Trop So Pulo. 2004;46(2): Hopkins KL, Kirchner M, Guerr B, Grnier SA, Lucrelli C, Porrero MC, et l. Multiresistnt Slmonell enteric serovr 4,[5],12:i:- in Europe: new pndemic strin?. Euro Surveill. 2010;15(22):pii= Aville from: eurosurveillnce.org/viewarticle.spx?articleid= Gossner CM, vn Cuterem D, Le Hello S, Weill FX, Terrien E, Tessier S, et l. Ntionwide outrek of Slmonell enteric serotype 4,[5],12:i- infection ssocition with consumption of dried pork susge, Frnce, Novemer to Decemer Euro Surveill. 2012;17(5):pii= Aville from: eurosurveillnce.org/viewarticle.spx?articleid= Agsn A, Kornlum J, Willims G, Prtt CC, Fleckenstein P, Wong M, et l. Profile of Slmonell enteric susp, enteric (suspecies I) Serotype 4,5,12 :i- Stins cusing food-orne infections in New York City. J Clin Microiol. 2002;40(6): Weill FX, Guesnier F, Guiert V, Timinouni M, Demrtin M, Polomck L, et l. Multidrug resistnce in Slmonell enteric serotype Typhimurium from humns in Frnce (1993 to 2003). J Clin Microiol. 2006;44(3): Lrsson JT, Torpdhl M, Petersen RF, Sorensen G, Lindstedt BA, Nielsen EM. Development of new nomenclture for Slmonell Typhimurium multilocus vrile numer of tndem repets nlysis (MLVA). Euro Surveill. 2009;14(15):pii: Aville from: spx?articleid= Guinrd A, Pouey J, Schwoeel V. Investigtion d une toxiinfection limentire collective limentire en milieu scolire en Hute-Gronne et dns le Trn [Investigtion of collective foodorne outrek in Hute-Gronne nd Trn schools].. Sint-Murice: Institut de veille snitire;apr p. 33. [Accessed 27 Sep 2012]. French. Aville from: invs.snte.fr/pulictions/2009/tic_hute_gronne_trn/ tic_hute_gronne_trn.pdf 15. Teunis PF, Ksug F, Fzil A, Ogden ID, Rotriu O, Strchn NJ. Dose-response modeling of Slmonell using outrek dt. Int J Food Microiol. 2010;144(2): Heymnn DL, Control of communicle diseses mnul. 19th ed, Wshington DC: Americn pulic helth ssocition, p Glynn JR, Brdley DJ. The reltionship etween infecting dose nd severity of disese in reported outreks of Slmonell infections. Epidemiol Infect. 1992; 109(3):