) R L. and L. ,5.6% and ¨ may oc- Ozdemir isolates (6.9%), L. monocytogenes L. innocua spp. in cheese L. ivanovii L. grayi L. monocytogenes and C). In manufacturing ◦ Streptococcus thermophilus Listeria spp. ( L. monocytogenes L. monocytogenes and Listeria 2012 Institute of Food Technologists , and 2.1% for Further reproduction without permission is prohibited C L. monocytogenes L. grayi spp. in homemade semisoft brined white in Baladi (boiled BWC) in Karak district isolates. The VITEK2 automated system Listeria spp. from cheese samples and a polymerase Lactobacillus bulgaricus ,4.9%for ) (Pintado and others 2005). In Jordan, the incidence (Arslan and Ozdemir 2008). In Sweden, Listeria spp., white cheese L. monocytogenes (0.3%). The pH values and salt concentrations of isolates. The overall prevalence of L. seeligeri Isolated from Brined BWC is a rennet-coagulated cheese (Al-Holy and others L. monocytogenes spp. in brined white cheese (BWC) sold in Jordan, and to ferent parts ofand the others globe 2005; (Loncarevic Wagner2008; and and Brito and others others others 2006; 2008; 1995;the Rahimi Arslan Pintado and incidence and others of 2010). Incheese Turkey, (BWC) was 9.2% for for ufacturing of halloumi andstarter culture shellal ( cheese, inis addition usually to added rennet, solution to is pasteurized maintained at milk. 10%Contamination to The 24% of salt for white these contentcur varieties cheese of of at with cheese. different brine processing stages from floor, packaging material, of boiled cheese,cheese, raw which milk is is boiledand used afterward akkawi to in cheese manufacture brinemilk are this solution. is very type used Pasteurized similar; of but in akkawi cheese these has types, a pasteurized bigger piece size. In man- welshimeri was isolated from 42% of softothers and semisoft 1995). cheeses In (Loncarevic and Portugal,raw 75% of ewe’s soft milk cheese wereL. samples positive made innocua from for rate of was 2% (Al-Tahiri and others 2008). 2012) thatPolychroniadou is 2008). Different types classified ofEast-Mediterranean BWC as region are including known soft in pasteurized, the boiled,halloumi, akkawi, to and shellal. In semihard general,adding white (Alichanidis rennet cheese is enzyme and manufactured to by warm milk (35 Listeria , to antimicrobials. Three hundred and fifty samples of 5 different have L. welshimeri Listeria causes and L. monocytogenes (2%), and is rarely pathogenic L. monocytogenes Listeria monocytogenes L. monocytogenes L. monocytogenes was isolated from 39 (11.1%) samples. Other isolated species were L. seeligeri L. seeligeri. L. monocytogenes L. monocytogenes ivanovii is a serious foodborne pathogen that has been isolated from different dairy food products. L. monocytogenes, L. grayi, L. . Vol. 77, Nr. 9, 2012 doi: 10.1111/j.1750-3841.2012.02877.x L and r (4%), L. monocytogenes L. ivanovii positive cheese samples ranged from 5.10 to 6.32 and 5.64 to 13.16, respectively. Listeria monocytogenes antimicrobial susceptibility, comprises 6 species: (2%), is a Gram-positive, facultative anaerobic, non-spore Journal of Food Science has been isolated from different kinds of cheeses from dif- Listeria monocytogenes Listeria trimethoprim/sulfamethoxazole, benzylpenicillin, ciprofloxacin, erythromycin, tetracycline,to and fosfomycin, rifampicin, oxacillin, but and resistant clindamycin. monocytogenes were sensitive or intermediate susceptible to imipenem, gentamicin, linezolid, teicoplanin, vancomycin, fusidic acid, L. innocua sample was 27.1%. determine the susceptibility of isolated Keywords: Abstract: chain reaction (PCR) technique waswas used used for for testing confirmation antimicrobial susceptibility of of Several foodborne outbreaks of listeriosisto have determine been the associated with occurrence consumption of of cheese. The aimstypes of of this BWC (akkawi, study boiled, were (11290-1) halloumi, pasteurized, procedure was and shellal) followed for were collected isolation from and a identification local market of in Jordan. The ISO Listeria listeriosis associated with the(17 consumption cases, 3 of died) camembert andnant cheese Mexican-style Hispanic cheese (8 females) cases, contaminatedbeen 7 reported with were (Johnsen preg- and others 2010;Listeria Jackson and others 2011). for humans (Cummins andan others infection 1994). called listeriosis thatimmunocompromised occurs people, predominantly in and elderly, Donachie pregnant 1997). This women disease (Lowdeath is characterized and rate by that aListeriosis relatively may high is reach often associated 40%ready-to-eat (RTE) with foods (Gandhi including consumption cheese. and Recently, of outbreaks of contaminated Chikindas 2007). innocua, L. ivanovii, L. welshimeri,is pathogenic for humans, while Direct inquiries to author Osaili (E-mail: [email protected]). M528 MS 20120173Al-Nabulsi, Submitted Taha, 2/5/2011, and ShakerFaculty Accepted of are Agriculture, 5/24/2012. with JordanAuthor Univ. Dept. Authors of Al-Holy of Science is Osaili, and Nutrition withHealth Technology, Irbid, Dept. and Sciences, 22110 of Food Hashemite Jordan. Clinical Univ., Technology, Dept. Nutrition Zarqa, of and 13115 Pathology Dietetics, and Jordan. Faculty Animalof Author Health, of Science Alaboudi Faculty Allied and of is Technology, Irbid, Veterinary with Applied Medicine, 22110 Jordan Sciences, Jordan. Univ. Al-Huson Author Univ. Al-Rousan College, is Al-Balqa’ with Applied Dept. Univ., Irbid, of Jordan. Introduction White Cheese in Jordan Tareq M. Osaili, Anas A. Al-Nabulsi,Walid Mohammad M. H. Al-Rousan, Taha, and Murad Reyad A. R. Al-Holy, Shaker Akram R. Alaboudi, Occurrence and Antimicrobial Susceptibility of forming rod-shaped bacteriumgenus (Larson and others 1999). The

M: Food Microbiology & Safety xrc TBE Ood t. aigtk,UK)a 37 at U.K.) Basingstoke, Ltd., (Oxoid, yeast (TSBYE) 0.6% with extract strains supplemented broth lyophilized soy These tryptone strains. in refreshed reference were standard as study this in and n etfoe nTBEwt 0 lcrla –20 at glycerol 20% with TSBYE in frozen kept and h ntytn o grsplmne ih06 fyatextract yeast of 0.6% 4 with at stored supplemented and (Oxoid) agar (TSAYE) monthly soy refreshed and tryptone grown were on cultures frozen the from tures i)splmne ihFae upeet(R16)(Oxoid) (SR0156E) 37 at supplement incubated Fraser and (Ox- with broth Fraser supplemented medium oid) enrichment secondary mL 10 to added E aoaor,Fac) h ooeaewsicbtdat incubated was homogenate The Mix, 30 (Easy France). circulator Laboratoire, stomacher using stomacher AES s in 30 for (Oxoid) U.K.) supplemented (Seward, (SR0166E) bag (Oxoid) supplement broth Half-Fraser with Half-Fraser primary g of medium mL 25 225 below: with enrichment homogenized as were followed sample cheese was each 2004) of (1996, 11290-1) (ISO ization h. 24 within stored at were analyzed Lab. samples under Microbiology and Technology. The Food and transferred the Science and to of Univ. box markets Jordan ice an the in from conditions purchased aseptic were approximately g) (each samples 150 period The 2011. the April to during 2011 governorates) January from (12 governorates collected were Jordan 31) all shellal: from and 115, pasteurized: 30, halloumi: 115, France), Listeria of identification and isolation, preparation, Sample samples BWC of Collection strains Bacterial Methods and Materials of susceptibility the and markets Jordanian monocytogenes the in sold BWC others and Rahimi all 2009). that indicated others and (2010) and (93.3%) (Harakeh oxacillin (90%) against penicillin resistance showed treatment. cheese therapeutic including of failure cause Recently, may community that represent problems may health isolates environment cells multiresistant Antimicrobial-resistant and particularly food, 1999). and cases, Courvalin clinical and sporadic (Charpentier from isolates for others and Durmaz 1999; others preservation and 2009). survive (Larson to BWC able of is processes it to concentrations, Due salt and 2006). perature, others of and (Temelli tolerance remarkable brine air, the room and production room, cloth, storage cheese cold knife, cutting curd vat, cheese of Occurrence tekdo ufc fLsei eetv gr(xodAa)supple- Agar) (Oxford Agar Selective Listeria of surface on streaked W nJra.Teeoe h betvso hssuywr to were study this of of prevalence objectives in the pathogen the determine Therefore, this of Jordan. occurrence in the BWC to are pertaining there data countries, different insufficient in products dairy especially products, vancomycin. to susceptible were isolates) (54 cheeses and h rcdr ecie yteIt.Ognzto o Standard- for Organization Intl. the by described procedure The boiled: 59, (akkawi: BWC of types 5 of samples 350 of total A monocytogenes L. niirba eitneof resistance Antimicrobial Although, ◦ o 4h fe ht . Lfo afFae rt was broth Half-Fraser from mL 0.1 that, After h. 24 for C hdccu equi Rhodococcus spp. tpyoocsaureus Staphylococcus .monocytogenes L. .monocytogenes L. sltst antimicrobials. to isolates .monocytogenes L. ◦ o 8h opu rmFae rt was broth Fraser from loopful A h. 48 for C AC 99 Mcoilgc)wr used were (MicroBiologics) 6939) (ATCC AC 64 Mcoilgc,Cedex, (MicroBiologics, 7644) (ATCC Listeria sltdfo ar-ae odproducts food dairy-based from isolated .monocytogenes L. Listeria .monocytogenes L. a enioae rmmn food many from isolated been has AC 52)(MicroBiologics), 25923) (ATCC p.ioae rmrwsepmilk sheep raw from isolated spp. ◦ C. nces . . . cheese in p.and spp. oeteep,tem- pH, extreme to .monocytogenes L. a enrecorded been has ◦ ◦ Cfor24 .Cul- C. L. in technique et aaaets,hmlssts,CM et n biochemical and test, oxidase CAMP test, test, Microbact motility by hemolysis staining, identification test, gram catalase to test, subjected were isolates fe 4t 8h upce ooisfo ahpae eestreaked Agar 37 were at plate, Listeria incubated each from and Chromogenic TSAYE colonies colonies Suspected into on h. green-blue 48 halo by to 24 opaque or after an halos by black surrounded by surrounded colonies Listeria suspected extract to used from was DNA U.S.A.) the Wis., kit, purification DNA Genomic eld n oddit h paau o nuain(35.5 incubation for apparatus, apparatus vacuum the into integrated loaded an and by sealed, suspensions as inoculated microbial test, was card with susceptibility The 0.45%). antimicrobial instructions. mL, manufacturer’s for by (3 described used solution the was saline and suspension strain sterile The reference in the emulsified of were colonies isolates of number sufficient inoc- ula, microbial the prepare To and trimethroprim/sulfamethoxazole. rifampicin, acid, fusidic fosfomycin, teicoplanin, tetracycline, vancomycin, linezolid, gentamicin, clindamycin, erythromycin, imipenem, ciprofloxacin, oxacillin, benzylpenicillin, timicrobials: for au- VITEK2 for card, the AST-P592 using (bioM antimicrobials system to tomated susceptibility their for used. in available not cus were that acid) fusidic fosfomycin,and (benzylpenicillin, antimicrobials those For rifampicin. and tetracycline, vancomycin, teicoplanin, erythromycin, linezolid, ciprofloxacin, clindamycin, isolates the gentamicin, of imipenem, susceptibility oxacillin, the to evaluate to used were 2007) for (CLSI Breakpoints trimethoprim/sulfamethoxazole. to for 2006) (CLSI study, Inst. this Standard monocytogenes Lab. In Clinical standards. by international defined the criteria of most by defined been ofimto of Confirmation ◦ of susceptibility Antimicrobial S02E n hooei itraSlcieSupplement Selective 35 at Listeria incubated and Supplement (Oxoid) Chromogenic (SR0226E) Differential and (ALOA) Listeria Agar (SR0228E) Brilliance Listeria with Chromogenic supplemented (SR0206E and Supplement (Oxoid) Selective supplement) Listeria Modified with mented eetdbsdo h ulse uloiesequence of a fragment amplify nucleotide DNA (5’- bp to were800 published used and typing was CCCGACAGTGGTGCTAGATT-3’) (5’-ACGAGTAACGGGACAAATGC-3’) the assay primers on (PCR) the reaction of based chain selected polymerase the instructions. ytm(e o 00 I-A,Clf,U.S.A.). UV Calif., documentation BIO-RAD, with gel 2000, visualized Doc the (Gel were with system photographed products Biosystems, and amplifications PCR (Applied transilluminator All The Veriti (2011). U.S.A.). thermocycler others a Calif., on and performed Osaili were and (2007) others )adraig lnclbekonsfor breakpoints Clinical reading. and C) N extraction. DNA .monocytogenes L. C procedure. PCR rtra rapit endb osyadohr(94 were (1994) other and Soussy by defined breakpoints criteria, Listeria p.clswr dnie nOfr grb grayish by Agar Oxford on identified were cells spp. inlA .monocytogenes L. xss h adi opsdo h olwn an- following the of composed is card The exists. eeue oeaut h ucpiiiyo h isolates the of susceptibility the evaluate to used were o.7,N.9 2012 9, Nr. 77, Vol. ee(ugadohr 03.Tepi of pair The 2003). others and (Jung gene .monocytogenes L. .monocytogenes L. eeec tanadBCioae eetested were isolates BWC and strain reference .aureus S. rexSA,MryLEol,Fac) The France). L’Etoile, Marcy S.A., erieux ´ N xrcinkt(rmg Wizard (Promega kit extraction DNA A .monocytogenes L. sltsacrigt h manufacturer’s the to according isolates TM inlA a sdbcuen pcfi card specific no because used was , itra1LKtSse (Oxoid) System Kit 12L Listeria AC 64 eeec tanand strain reference 7644) (ATCC r ◦ .monocytogenes L. eea ecie yLuand Liu by described as gene ora fFo Science Food of Journal o 8t 4h l suspected All h. 24 to 18 for C sltsb PCR by isolates ◦ .monocytogenes L. seicpiesfor primers -specific o 8h Presumptive h. 48 for C Listeria and Staphylococci Staphylococ- aenot have M529 ± 1.0 L.

M: Food Microbiology & Safety L. 0.5 0.25 ≤ ≤ (ATCC g/mL. All µ g/mL, van- µ 10 2 4 25 96 08 . . . . . spp. Similarly, the ≤ L. monocytogenes 2 2 1 1 2 isolates are shown 0.5 ± ± ± ± ± ≤ g/mL, ciprofloxacin in dairy products and µ 86 35 64 51 16 . . . . . g/mL, rifampicin Listeria L. monocytogenes µ 0.5 g/mL, clindamycin 1 ≤ µ spp. in BWC reported in this ≤ L. monocytogenes L. monocytogenes reported in our study is lower than in different types of BWC sold in 0.25 contaminated with ≤ Listeria spp. Pintado and others (2005) reported L. monocytogenes g/mL, teicoplanin µ Listeria isolates were sensitive to 6 single antimicrobials: g/mL, tetracycline positive cheese samples were 6.11 and 6.86% for L. monocytogenes L. monocytogenes µ L. monocytogenes 0.260.180.270.190.07 6 7 5 7 13 g/mL, erythromycin ± ± ± ± ± µ Despite of the risk of The antimicrobial susceptibility of g/mL, and trimethoprim/sulfamethoxazole g/mL, linezolid 2 antimicrobials, while 5 isolatesantimicrobials (Figure were 1). multiresistant to 3 or more µ L. monocytogenes imipenem, gentamicin, linezolid,trimethoprim/sulfamethoxazole; teicoplanin, and vancomycin, more and thanlates 92% were of sensitive theciprofloxacin, to iso- erythromycin, 5 tetracycline, single andthe isolates rifampicin. antimicrobials: were resistant All benzylpenicillin, to fosfomycin. of isolates Also, 92% were and resistant 56% of toThis the oxacillin study and found clindamycin, also respectively. that 35 isolates were resistant to 1 or 2 incidence of 1 µ comycin 1 its serious health implications,currence little information of exists onJordan. the The oc- prevalence of study (27%) iscountries. lower Guner than and that Telli120 (2011) reported samples reported of from 4 that different other 50 typescontaminated of developing with (42%) semihard cheese out in of Turkey were that 47 (75%) out ofewe’s milk 63 in tested Portugal soft were cheese positive samples for made from raw 7644) and the 39in confirmed Table 3. Thebials out reference of the strain 15concentrations was tested antimicrobials. sensitive The were: minimum to inhibitory 10 gentamicin antimicro- Discussion pH values and salt6.08 concentrations and for 7.61% eachcheese, for 5.89 type akkawi and of 6.83% cheese, cheesepasteurized for 6.02 were cheese, halloumi and cheese, and 6.16 9.71%spectively. 5.28 The and for and 7.94% average boiled 11.04% for pHmonocytogenes for values shellal and cheese, saltakkawi re- concentrations cheese, 6.23 of and 7.35%for for halloumi boiled cheese, cheese, 5.64 6.32 and5.10 and 5.64% and 7.51% 13.16% for for shellal pasteurized cheese, cheese, respectively (Table and 2) Antimicrobial susceptibility of SD) of BWC samples. L. in- ± ,24sam- 0.00292) / L. welshimeri × 3 isolates were Gram 46.11 17623548 6.23 5.64 6.32 5.10 . . . . . 1 4 1 2 2 , 14 samples (4%) were C for 8 h. After that, 25 ◦ ± ± ± ± ± L. monocytogenes L. grayi L. innocua L. ivanovii L. monocytogenes L. seeligeri L. welshimeri Listeria 61 71 83 94 04 . . . . . in cheese . . . L. grayi Vol. 77, Nr. 9, 2012 spp. isolated from different types of BWC by conventional methods. r , 7 samples (2%) were contaminated isolates were confirmed molecularly Listeria in the examined BWC was 11.1%. The spp. in BWC 0.250.320.420.29 7 0.14 9 6 7 11 (titrated volume of AgNO ± ± ± ± ± spp. All suspected = L. ivanovii Average Average salt Average pH value of samples Average salt concentration (%) of samples 100% (Pearson 1985). L. monocytogenes Listeria × , 7 samples (2%) were contaminated with Listeria L. monocytogenes Average pH value and salt concentration (Mean Journal of Food Science L. monocytogenes L. seeligeri , and 1 sample (0.3%) was contaminated with Salt content (%) The pH values of the BWC samples ranged from 4.69 to 6.68 Based on the results of the conventional (ISO) method, 95 sam- The pH values of cheese samples were determined using pH Salt content in cheese samples was determined using Pearson’s prevalence among different cheese varieties was 6for out of akkawi 59 cheese (10.2%) samples, 12 outsamples, of 115 3 (10.4%) out for boiled of cheese of 30 115 (10%) (12.2%) for for(12.9%) halloumi for pasteurized cheese shellal cheese cheese samples, samples. samples, 14 and out 4 out of 31 ples (6.9%) were contaminated with contaminated with with nocua (Table 1). Thirty-nine isolates (93%)identified out of the 42 presumptively (wt. of sample) mL distilled water was addedmixed thoroughly. A to few the droplets (0.5 ashed mL sample maximum)chromate of in (0.5 potassium a N) beaker were and the added to sample the was sampleSalt titrated as content indicator. against (%) Finally, silver inequation: nitrate the sample solution was (0.05 determined N). by the following M530 Table 2 – pH values and salt contents (%) of BWC samples Table 1–Identification of Results Prevalence of pH determination Occurrence of Salt content determination and salt concentrations ranged from 2.15% to 18.7%. The average using PCR technique. Accordingly, the overallfirmed prevalence of con- samples (12%) were contaminated with ples (27.1%) out of thepresence examined of 350 BWC samplespositive, motile, revealed the oxidase negative, and catalase positive. Forty-two meter (Jenway, U.K.) by immersing theimately electrode 50 into g an piece approx- of cheese. was ashed in a muffle furnace oven at 550 procedure (Pearson 1985) as follows: 1 g of each cheese sample Type of BWC pH value concentration (%) contaminated with PasteurizedShellal 6.16 5.28 AkkawiBoiledHalloumi 6.08 5.89 6.02 Type of BWCAkkawiBoiled Nr. ofHalloumi samples PasteurizedShellalTotal 18 32 31 6 8 6 95 10 5 2 1 1 24 4 1 1 0 4 7 3 6 0 1 14 6 14 15 3 4 42 1 1 3 0 2 7 0 0 1 0 0 1

M: Food Microbiology & Safety rmtorm Sulfamethoxazole Trimethoprim/ Rifampicin Acid Fusidic Fosfomycin Tetracycline Vancomycin Teicoplanin Linezolid Clindamycin Erythromycin Ciprofloxacin niirba I ag ( range MIC R S Gentamicin Imipenem Oxacillin Benzylpenicillin Antimicrobial ,Sniie ,Itreit;R Resistant. R, Intermediate; I, Sensitive; S, – 3 D’Amico Table and (2004) others and Kabuki 2006). surfaces. others contaminated and cold (Temelli air, solution room monocytogenes brine production and cloth, room, cheese storage knife, cheese cutting material, packaging curd floor, vat, from be may plants processing in with BWC of Contamination respectively. 1.4%, the that reported (1998) others of and occurrence Silva 11%. of rate study current with contamination that reported with contaminated They were samples) monocytogenes (2005). (29 samples others cheese the and of 46% Pintado by reported that of Occurrence aa,Jra.Te eotdta h vrg curneof occurrence average the that monocytogenes reported They Jordan. Karak, of prevalence and The (Arslan 10.7%. 9.2% was Brazil Janeiro, monocytogenes de Rio in sold n tes(08 isolated (2008) others and and transportation Arslan and 2008; mas- storage others with during and animals (Al-Tahiri handling from milk through contaminated and be titis could milk raw where 2010). (Mahmoodi 6.7% reached Iran, Noorabad, in plants monocytogenes L. otmnto fces by cheese of Contamination iiu niioycnetain(I)( (MIC) concentration inhibitory Minimum te tde aerpre oe eeso cheese of levels lower reported have studies Other . , nhmmd ht heei etr ukywas Turkey Western in cheese white homemade in a eesl pedb ietfo otc with contact food direct by spread easily be can .monocytogenes L. .ivanovii L. .monocytogenes L. nwieces ntaiinldiymanufacturing dairy traditional in cheese white in zei 08.Adtoal,teicdneof incidence the Additionally, 2008). Ozdemir ¨ .monocytogenes L. ,and Listeria Listeria n13smlso ye fcheese of types 3 of samples 103 in ≤ .innocua L. ≤ 0.5/9.5 ≤ ≤ ≤ ≤ ≤ ≤ ≤ ≤ ≤ ≤ ≤ ≤ ≤ rapitN.o slts(%) isolates of Nr. Breakpoint 0.25 0.5 0.5 32 1 2 . o2S3(0)00 0 0 0 39(100) 39(100) S I 2 to 0.5 4 to 1 – – 4 2 8 4 1 4 4 2 p.fo a he ikin milk sheep raw from spp. nces . . . cheese in htcmsi iewt the with line in comes that p.mysatfo h farm the from start may spp. zei 08.Al-Tahiri 2008). Ozdemir ¨ ≥ a 15,34,and 3.4%, 11.5%, was > > > ≥ ≥ ≥ ≥ ≥ ≥ ≥ ≥ ≥ /61 910 0 0 39(100) S 10 4/76 61t 6S3(5 (5) 2 0 0 0 37(95) 39(100) S S 16 to 1 0.5 16 32 61S3(0)00 0 39(100) S 1 16 218R003 (100) 39 (3) 1 0 (85) 33 0 5(13) R I 16 to 0.5 128 16 32 600 o05S3(5 5 0 (5) 2 37(95) S 0.5 to 0.03 16 . o3 69)1()2(5) 2 (3) 1 36(92) S 32 to 0.5 4 .5t 64)1()2 (56) 22 (3) 1 16(41) S 8 to 0.25 4 .5t 69)3()0 (8) 3 36(92) S 2 to 0.25 8 . o2S3(7 3 (0) 0 (3) 1 38(97) S 2 to 0.5 4 . 910 0 (92) 36 0 39(100) 0 3(8) S R 0.5 4 to 0.25 8 4 .monocytogenes L. µ /L n estvt of sensitivity and g/mL) µ L. L. L. L. /L AC,74)SIR I S 7644) (ATCC, g/mL) icnl fe 5do trg t4 at storage of d 15 is after which nificantly cheese, (2009) although boiled others so- that and for reported brine Durmaz temperature. expect in room at preserved preserved refrigerators were usually in cheese white and In of lutions microorganisms. types and of all cheese white growth study, from our the brine released supporting nutrients to possibly in repeatedly therefore rich used brine often making are cheese, brines cheese mercial be- plants dairy surfaces. in contaminated are contamination which of drains, sites cause and major floors the like considered surfaces contact nonfood that from reported (2009) Donnelly and rmces eddt emr atrssatta tan rmother storage. from strains of than salt-resistant d more be 90 that to tended during indicated cheese from solution (2003) brine others the and in Faleiro survive to able was rn ouin o ogtm eid Lro n tes1999); to contamination others of transfer source and by potential a (Larson cheeses be periods possibly can time brine long hence for solutions brine 2002). (Samelis concentrations others salt and high of tolerate range to growth capability remarkable and survival the monocytogenes within L. are samples cheese itive h Hvle n atcnetain of concentrations salt and values pH The ucpiiiyof Susceptibility .monocytogenes L. .monocytogenes L. o.7,N.9 2012 9, Nr. 77, Vol. Jyadohr 2005). others and (Jay .monocytogenes L. .monocytogenes L. .monocytogenes L. .monocytogenes L. multiantimicrobial-resistant of 1–Percent Figure aiysrasb ietfo otc with contact food direct by spreads easily .monocytogenes L. sltst antimicrobials. to isolates r ora fFo Science Food of Journal .monocytogenes L. rmbiet hee Com- cheese. to brine from uvvdi ifrn cheese different in survived ◦ isolates. nbie(5 al,it NaCl), (15% brine in C .monocytogenes L. ouaindcesdsig- decreased population .monocytogenes L. .monocytogenes L. a isolated was xiisa exhibits isolates M531 pos-

M: Food Microbiology & Safety in ¸aise Liste- Liste- .Intl. species Listeria Listeria ´ eFranc ´ isolated from et spp. in small- Listeria mono- species in raw Listeria Listeria monocy- spp. in homemade in various semi-hard Listeria in commercial cheese Listeria in cheese produced in Listeria monocytogenes spp. Antimicrob Agents Listeria Listeria monocytogenes and listeriosis. Vet J 153:9–29. infection in a patient with AIDS. Listeria in raw milk and dairy products in Listeria monocytogenes spp. and antibiotic susceptibility of . Int J Food Microbiol 128:497–500. . J Microbiol Methods 71:133–40. Listeria monocytogenes Listeria monocytogenes Listeria Listeria monocytogenes Listeria ivanovii ´ e de l’Antibiogramme de la. Soci Listeria monocytogenes : a foodborne pathogen that knows how to survive. Int Listeria monocytogenes Listeria monocytogenes isolates. Appl Environ Microbiol 74:4954–61. Listeria monocytogenes Listeria isolated from soft cheese. Food Microbiol 22:79–85. C in vacuum packages. J Food Prot 64:1722–9. ◦ isolated from dairy-based food products. Sci Total Environ 407:4022–7. spp. isolated from raw meat and retail foods. Food Control 21:708–13. isolated from raw chicken and ready-to-eat chicken products in Jordan. in Latin style fresh-cheese processing plants. J Dairy Sci 87:2803–12. . J Food Agric Environ 7:11–3. infection with short incubation period in a tertiary care hospital. J Infect isolates from 50 small-scale Austrian cheese factories. J Food Prot 9:1297–303. isteria Listeria monocytogenes on frankfurters using oligonucleotide primers targeting the genes encoding growninliquidmediaandonprocessedmeatsurfaces.ApplEnvironMicrobiol with combined antimicrobials following postprocess contamination and extended Listeria monocytogenes ¨ associated with Mexican-style cheese made from pasteurized milk among pregnant, Ozdemir F. 2008. Prevalence and antimicrobial resistance of Listeria monocytogenes monocytogenes internalin AB. J Food Prot 66:237–41. Listeria monocytogenes brines. J Dairy Sci 82:1860–8. virulence-specific determination of soft and semi-soft cheeses in retail outlets in Sweden. Int J Food Microbiol 26:245–50. Hispanic women. J Food Prot 74:949–53. ed. New York: Springer. p 591–618. ria monocytogenes 61:465–70. stuffs: horizontal methodStandard for ISO the 11290-1. Geneva, detection Switzerland: and Intl. Organization enumeration for of Standardization. haemolysis test, and inclusionSwitzerland: of Intl. precision Organization data. for ISO Standardization. 11290-1: 1996/Amd 1: 2004.E, Geneva, Saathoff-Huber L, Hainstocktogenes L, Fagan RP. 2011. Multistate outbreak of cheeses from different regions in Turkey. J Anim Vet Advof 10:1890–4. cheese and other foods. Int J Food Microbiol 84:207–16. J Food Microbiol 113:1–15. sources during Turkish white cheese production. Food Control 17:856–61. ria monocytogenes de Microbiologie. 1994.breakpoints Definition for and bacteria in determination France. of Eur J in Clin vitro Microbiol Infect antibiotic Dis susceptibility 13:238–46. scale artisan cheese processing facilities: a methods comparison. JListeria Food monocytogenes Prot 72:2499–507. Rio de Janeiro, Brazil. J Food Prot 61:354–6. monocytogenes 62:3088–93. white cheese. Food Control 19:360–63. Beltran JMS, Call JE, Liumilk Y, and Proto-Feet Minas Frescal ACS, cheese Luchansky and JB. contaminatedand 2008. dairy sources plant Retail to of survey establish of prevalence, relatedness, Brazilian Chemother 43:2103–9. disk susceptibility testing of(M45-A). Wayne, infrequently Pa.: Clinical isolated and or Laboratory Standards fastidious Inst. bacteria:susceptibility approved testing: guideline seventeenth informational supplement (M100-S17).and Wayne, Pa.: Clinical Laboratory Standards Inst. antimicrobial resistance of foodborne J Infect 28:89–91. Listeria monocytogenes Food Control 22:586–90. Churchill. susceptibility of tion of isolated from milk and dairy products in Iran. Foodcytogenes Control 21:1448–52. storage frankfurters at 4 sheep milk. Int J Dairy Technol 61:347–51. Noorabad, Iran. J Anim Vet Adv 9:16–9. Kabuki DY, Kuaye AY, Wiedmann M, BoorLarson KJ. AE, 2004. Johnson EA, Molecular Nelson JH. subtyping 1999. Survival and of tracking of Liu D, Lawrence M L, Austin FW,Loncarevic Ainsworth S, AJ. Danielsson-Tham ML, 2007. Tham A W. multiplex 1995. PCR Occurrence for of species- and Jay JM, Martin LJ, David GA. 2005. Foodborne listeriosis.Johnsen In: BO, Modern Lingaas food microbiology. E, 7th Torfoss D, Strøm EH, NordøyJung I. YS, Frank 2010. JF, A Brackett RE, large Chen outbreak J. of 2003. Polymerase chain reaction detection of Intl. Organization for Standardization (ISO). 1996. Microbiology of food andIntl. animal Organization feeding for Standardization (ISO). 2004. Modification of the isolation media and the Jackson KA, Biggerstaff M, Tobin-D’angelo M, Sweat D, Klos R, Nosari J, Garrison O, Boothe Harakeh S, Saleh I, Zouhairi O, Baydoun E, Barbour E, Alwan N. 2009. Antimicrobial resistance Gandhi M, Chikindas ML. 2007. Guner A, Telli N. 2011. A survey on the presence of Temelli S, Anar S, Sen C, AkyuvaWagner P. M, Eliskases-Lechner 2006. F, Rieck Determination P, Hein of I, microbiological Allerberger R. contamination 2006. Characterization of Durmaz H, Aygun O, Ardic M. 2009. The effectFaleiro of ML, cheese Andrew PW, brine Power concentrations D. on 2003. survival Stress of response of Smith LT. 1996. Role of osmolytes in adaptation of osmotically stressed and chill-stressed Soussy CJ, Cluzel R, Courvalin P; the Comit Brito JR, Santos EMP, Arcuri EF, Lange CC, Brito MAVP, Souza GN, Cerqueira MM PO, Clinical and Laboratory Standards Inst. (CLSI). 2006. Methods for antimicrobialClinical dilution and and Laboratory Standards Inst. (CLSI). 2007. Performance Standards for antimicrobial Conter A, Paludi D, Zanardi E, Ghidini S, Vergara A, Ianieri A.D’Amico 2009. DJ, Donnelly Characterization CW. of 2009. Detection, isolation, and incidence of Silva MCD, Hofer E, Tibana A. 1998. Incidence of Low JC, Donachie W. 1997. A review of Pearson D. 1985. The chemical analysis ofPesavento foods. G, 6th Ducci ed. B, Gloucester Nieri Place, D, London: Comodo JPintado CMBS, N, and Oliveira A Lo A, Pampulha Nostro ME, A. Ferreira MASS. 2010. 2005. PrevalenceRahimi Prevalence E, and and Ameri characteriza- antibiotic M, Momtaz H. 2010. Prevalence and antimicrobial resistanceSamelis of J, Sofos JN, Kain ML, Scanga JA, Belk KE, Smith GC. 2002. Control of Arslan S, Charpentier E, Courvalin P. 1999. Antibiotic resistance in Cummins AJ, Fielding AK, McLauchlin J. 1994. Mahmoodi MM. 2010. Occurrence of Osaili T, Alaboudi A, Nesiar E. 2011. Prevalence of Al-Tahiri R, Omar S, Rewashdeh A. 2008. A study of the occurrence of Lis- ¨ L. mono- Ozdemir L. monocy- (22%) from L. monocyto- L. monocyto- isolates in this is gradually turn- isolates (39) showed C. Salt is used to control ¨ ◦ Ozdemir (2008) reported to imipenem, teicoplanin, C). Larson and others (1999) L. monocytogenes in cheese . . . ◦ L. monocytogenes Vol. 77, Nr. 9, 2012 r L. monocytogenes can survive in commercial cheese L. monocytogenes ) (Pesavento and others 2010). That to tolerate high salt concentrations is L. monocytogenes isolate that was resistant to 2 antimicrobials. isolates were resistant to fosfomycin and oxacillin, Staphylococcus L. monocytogenes L. monocytogenes spp. isolated from homemade white cheese were and in brined white cheese by a combination of nisin and heat. Food Control 23: L. monocytogenes isolates in this study were sensitive to these antimicrobials. Journal of Food Science from homemade cheese, but they found only 1 (out of 13) to antimicrobials. All of Listeria , respectively, (Charpentier and Courvalin 1999). All The majority (92% to 100%) of This work received financial support from the Deanship of Sci- The results of this study demonstrated that BWC might pos- varieties of East-Mediterranean countries: a review. Dairy Sci Technol 88:495–510. teria innocua 48–53. ability of due to its abilitylutes of called intracellular osmolytes. These accumulationosmolarity, solutes of so water counterbalance compatible loss the from so- the external 1996). bacterial cell is prevented (Smith the growth of pathogens in food and to enhance the flavor. The reported that brine (23.8% NaCl) for over 259 d at 4 M532 References Al-Holy MA, Al-Nabulsi A, Osaili TM, Ayyash MM, Shaker RR. 2012.Alichanidis Inactivation E, of Polychroniadou A. 2008. Characteristics of major traditional regional cheese Acknowledgment Conclusions Occurrence of sources, even at low temperature (8 entific Research, Jordan Univ. ofJordan. Science and Technology, Irbid, other food safety programscheese should processing plants be to implemented prevent contamination effectivelyfoodborne and in exposure pathogens. to The useshould of be antimicrobials monitored at and the controlled. farm level sess a risk for consumer health,patients in particular, and immunocompromised pregnant women in Jordan. Sanitationating Standard Procedures Oper- (SSOPs), Good Manufacturing PracticesHazard (GMP), Analysis and Critical Control Point (HACCP) system, and milk and dairy(2008) products could including not cheese. isolatetogenes Arslan a multiantimicrobial-resistant and L. monocytogenes ity of alland isolates vancomycin. of Similarly, Arslanthat and icin remain the choicetion for of treatment sulphamethoxazole and of trimethoprim listeriosis. ischoice considered The the of 2nd combina- treatment. Vancomycintreat and bacteraemia and erythromycin pregnant are womengenes infected used with to cytogenes The results of antimicrobial resistance test confirmed susceptibil- study were sensitive to 11 antimicrobials. Penicillin plus gentam- L. monocytogenes respectively. Similar toisolated our multiantimicrobial-resistant finding, Rahimi and others (2010) antimicrobial-resistant genes from Gram positiveEnterococcus bacteria (that is, probably justified the sensitivitygenes of the majorityresistance to of fosfomycin, and 92.3%tant (36) to of oxacillin. the These isolates results wereConter are resis- and in agreement others with (2009) the who results reported of that 96.8% and 97.6% of generally sensitive andity some to displayed gentamicin, intermediate vancomycin,and susceptibil- trimethoprim/sulfamethoxazole, amoxicillin-clavulanic acid. ing into antimicrobial-resistant microbe because of the uptake of

M: Food Microbiology & Safety