FOODBORNE PATHOGENS AND DISEASEVolume 2, Number 2, 2005© Mary Ann Liebert, Inc.

Review

Foodborne Pathogens in Milk and the Dairy FarmEnvironment: Food Safety and

Public Health Implications

S.P. OLIVER,1 B.M. JAYARAO,2 and R.A. ALMEIDA1

ABSTRACT

Milk and products derived from milk of dairy cows can harbor a variety of microorganisms and can be importantsources of foodborne pathogens. The presence of foodborne pathogens in milk is due to direct contact with con-taminated sources in the dairy farm environment and to excretion from the udder of an infected animal. Mostmilk is pasteurized, so why should the dairy industry be concerned about the microbial quality of bulk tank milk?There are several valid reasons, including (1) outbreaks of disease in humans have been traced to the consump-tion of unpasteurized milk and have also been traced back to pasteurized milk, (2) unpasteurized milk is con-sumed directly by dairy producers, farm employees, and their families, neighbors, and raw milk advocates, (3) un-pasteurized milk is consumed directly by a large segment of the population via consumption of several types ofcheeses manufactured from unpasteurized milk, (4) entry of foodborne pathogens via contaminated raw milk intodairy food processing plants can lead to persistence of these pathogens in biofilms, and subsequent contamina-tion of processed milk products and exposure of consumers to pathogenic bacteria, (5) pasteurization may not de-stroy all foodborne pathogens in milk, and (6) inadequate or faulty pasteurization will not destroy all foodbornepathogens. Furthermore, pathogens such as Listeria monocytogenes can survive and thrive in post-pasteurizationprocessing environments, thus leading to recontamination of dairy products. These pathways pose a risk to theconsumer from direct exposure to foodborne pathogens present in unpasteurized dairy products as well as dairyproducts that become re-contaminated after pasteurization. The purpose of this communication is to review liter-ature published on the prevalence of bacterial foodborne pathogens in milk and in the dairy environment, and todiscuss public health and food safety issues associated with foodborne pathogens found in the dairy environ-ment. Information presented supports the model in which the presence of pathogens depends on ingestion of con-taminated feed followed by amplification in bovine hosts and fecal dissemination in the farm environment. Thefinal outcome of this cycle is a constantly maintained reservoir of foodborne pathogens that can reach humans bydirect contact, ingestion of raw contaminated milk or cheese, or contamination during the processing of milk prod-ucts. Isolation of bacterial pathogens with similar biotypes from dairy farms and from outbreaks of human dis-ease substantiates this hypothesis.

115

INTRODUCTION

MORE THAN 200 known diseases are trans-mitted through food by a variety of

agents that include bacteria, fungi, viruses, andparasites. According to public health and foodsafety experts, each year millions of illnesses inthe United States and throughout the world can

1Food Safety Center of Excellence and Department of Animal Science, The University of Tennessee, Knoxville, Ten-nessee.

2Department of Veterinary Science, The Pennsylvania State University, University Park, Pennsylvania.

be traced to foodborne pathogens. While thefood supply in the United States is one of thesafest in the world, the Centers for DiseaseControl and Prevention (CDC, 2003, 2004) esti-mates that 76 million people get sick, more than300,000 are hospitalized, and 5,000 die eachyear from foodborne illness. The risk of food-borne illness has increased markedly over thelast 20 years, with nearly a quarter of the pop-ulation at higher risk for illness today. Conse-quently, preventing illness and death associ-ated with foodborne pathogens remains amajor public health challenge. Furthermore,food safety is a global issue, and an increase inimport and export of food products could leadto introduction and establishment of new dis-eases in geographical areas that have never ex-perienced the foodborne pathogens.

The purpose of this communication is to re-view literature published on the prevalence offoodborne pathogens, primarily Campylobacterjejuni, Shiga toxin–producing E. coli (STEC),Listeria monocytogenes, and Salmonella, in milkand in the dairy environment, and to discusspublic health and food safety issues associatedwith foodborne pathogens found in the dairyenvironment.

PREVALENCE OF FOODBORNEPATHOGENS IN MILK

Several surveys have detected foodbornepathogens in bulk tank milk (Davidson, 1989;Doyle and Roman, 1982; Farber et al., 1988; Fe-dio and Jackson, 1990; Hassan et al., 2000; Jayarao

and Henning , 2001; Liewen and Plautz, 1988;Lovett et al., 1983, 1987; McEwen et al., 1988; Mc-Manus and Lanier, 1987; Muraoka et al., 2003;Murinda et al., 2002a,b, 2004a,b; Rohrbach et al.,1992; Slade et al., 1988; Steele et al., 1997; VanKessel et al., 2004; Waak et al., 2002). Results ofthose studies have shown clearly that the preva-lence of foodborne pathogens, including C. je-juni, STEC, L. monocytogenes, and Salmonella spp.in milk, varies considerably (Tables 1 and 2).

The prevalence of foodborne pathogens inmilk is influenced by numerous factors such asfarm size, number of animals on the farm, hy-giene, farm management practices, variation insampling and types of samples evaluated, dif-ferences in detection methodologies used, geo-graphical location, and season. However, inspite of the variation, all of these surveysdemonstrated quite clearly that milk can be amajor source of foodborne pathogens of humanhealth significance.

Rohrbach et al. (1992) reported that the fre-quency of isolation of foodborne pathogensfrom 292 bulk tank milk samples from dairiesin east Tennessee and southwest Virginia was12.3% for C. jejuni, 8.9% for Salmonella species,4.1% for L. monocytogenes, and 15.1% forYersinia enterocolitica. One or more foodbornepathogens were isolated from 32.5% of bulktank milk samples evaluated. One of the fourfoodborne pathogens was isolated from 73 of95 positive samples, and 22 samples containedtwo or more foodborne pathogens. Grade clas-sification of the dairy, milking facilities, barntype, milking hygiene, reported incidence ofclinical mastitis among cows, or the number of

OLIVER ET AL.116

TABLE 1. SURVEYS ON THE ISOLATION OF CAMPYLOBACTER JEJUNI AND SHIGA

TOXIN–PRODUCING ESCHERICHIA COLI FROM BULK TANK MILK

Foodborne pathogen Isolation rate (%) Reference

Campylobacter jejuni 0.9 Doyle and Roman (1982)1.5 Lovett et al. (1983)0.4 McManus and Lanier (1987)1.2 Davidson et al. (1989)

12.3 Rohrbach et al. (1992)0.5 Steele et al. (1997)9.2 Jayarao and Henning (2001)

Shiga toxin–producing 0.9 Steele et al. (1997)Escherichia coli 3.8 Jayarao and Henning (2001)

0.8 Murinda et al. (2002b)

cows per farm were not significantly associatedwith the isolation of foodborne pathogens inbulk tank milk. Of 84 dairy producers whoused teat disinfection and antibiotic dry cowtherapy that were classified as having goodmilking hygiene, 29 (35%) had bulk tank milkcontaminated with foodborne pathogens com-pared to 12 of 29 (31%) dairies with poor milk-ing hygiene (odds ratio 1.2, p � 0.7). Almost35% of dairy producers who participated, in-dicated that they consumed raw milk producedon their farm, and 25% of the bulk tank milksfrom these farms were contaminated with oneor more foodborne pathogens (Rohrbach et al.,1992).

In a similar study, bulk tank milk from 131dairy herds in eastern South Dakota and west-ern Minnesota was examined for the presenceof foodborne pathogens (Jayarao and Henning,2001). Thirty-five of 131 (26.7%) bulk tank milksamples contained one or more species of path-ogenic bacteria. Campylobacter jejuni, STEC, L.monocytogenes, Salmonella spp., and Y. enteroco-litica were detected in 9.2%, 3.8%, 4.6%, 6.1%,and 6.1% of bulk tank milk samples, respec-tively. Isolates of Salmonella belonged to “O”serogroups D (n � 4), B (n � 2), C (n � 1), and

E (n � 1). All six isolates of L. monocytogeneswere identified as O antigen type 1. Four of fiveisolates of E. coli encoded for the Shiga-toxin 2gene, while one strain encoded for the Shiga-toxin 1 gene. Escherichia coli O157:H7 was notisolated from bulk tank milk samples. Manu-facturing grade raw milk producers were at ahigher risk (odds ratio 4.98; confidence inter-val, 1.96–12.22) of having one or more food-borne pathogens in their bulk tank milk thanwere Grade A milk producers. Twenty-one of79 (26.6%) dairy producers who consumed rawmilk produced on their farm had one or morepathogenic bacteria in their bulk tank milk.

More recently, Van Kessel et al. (2004) re-ported results on the prevalence of foodbornepathogens in bulk tank milk samples obtainedas part of the National Animal Health Moni-toring System Dairy 2002 Survey. The objectiveof this study was to determine the nationalprevalence of Salmonella, L. monocytogenes, andfecal coliforms in bulk tank milk in the UnitedStates. Bulk tank milk samples (n � 861) werecollected from farms in 21 states. Coliformswere detected in 95% (818 of 860) of samples,and the average somatic cell count (SCC) was295,000 cells/ml. Twenty-two samples (2.6%)

DAIRY FOOD SAFETY 117

TABLE 2. SURVEYS ON THE ISOLATION OF LISTERIA MONOCYTOGENES

AND SALMONELLA SPP. FROM BULK TANK MILK

Foodborne pathogen Isolation rate (%) Reference

Listeria monocytogenes 4.2 Lovett et al. (1987)1.3 Farber et al. (1988)5.4 Slade et al. (1988)4.0 Liewen and Plautz (1988)1.6 Davidson et al. (1989)1.9 Fedio and Jackson (1990)4.1 Rohrbach et al. (1992)2.7 Steele et al. (1997)4.6 Jayarao and Henning (2001)

12.6 Hassan et al. (2000)1.0 Waak et al. (2002)

4.9 to 7.0 Muraoka et al. (2003)6.5 Van Kessel et al. (2004)

Salmonella spp. 4.7 McManus and Lanier (1987)2.9 McEwen et al. (1988)8.9 Rohrbach et al. (1992)0.2 Steele et al. (1997)6.1 Jayarao and Henning (2001)1.5 Hassan et al. (2000)2.2 Murinda et al. (2002a)2.6 Van Kessel et al. (2004)

were culture-positive for Salmonella, and nineserotypes were identified: Montevideo (n � 7),Newport (n � 4), Muenster (n � 2), Melea-gridis (n � 2), Cerro (n � 2), 44:Z36 (Z38) (n �2), Dublin (n � 1), Anatum (n � 1), and 9,12:nonmotile (n � 1). Listeria monocytogenesserotypes 1/2a, 1/2b, 3b, 4b, and 4c were iso-lated from 56 (6.5%) of samples; 93% wereserotypes 1/2a, 1/2b, and 4b, the most com-mon human clinical isolates. There were no ap-parent relationships between SCC or specificplate count and incidence of Salmonella or L.monocytogenes.

Another pathogen that is found frequently inbulk tank milk and is a significant cause of mas-titis in dairy cows throughout the world isStaphylococcus aureus. The bovine mammarygland can be a significant reservoir of entero-toxigenic strains of S. aureus. Enterotoxins pro-duced by enterotoxigenic strains of S. aureus areclassified according to serotypes into A–Hgroups and toxic shock syndrome toxin (TSST).The frequency of enterotoxigenicity amongststaphylococcal strains is highly variable (Geni-georgis, 1989; Mossel and Van Netten, 1990).Studies on S. aureus isolated from cows showedenterotoxigenicity ranging from 0 to 56.5%(Bennet et al., 1986; Castro et al. 1986; Kenny etal., 1993; Masud et al., 1993; Ruzickova, 1994).TSST was detected in S. aureus isolated in milkfrom cows with clinical and subclinical masti-tis, and in farm bulk tank milk (Takeuchi et al.,1998). Enterotoxigenic S. aureus was isolatedfrom raw milk samples at a milk cooperativein Kenya (Ombui et al., 1992) and in bulk milkcollected from dairy farms in Trinidad (Ade-siyun et al., 1998). It was inferred from thesestudies that bulk tank milk was a potentialsource of enterotoxigenic S. aureus in milk andmilk products, and may constitute a health haz-ard to consumers. Enterotoxigenic strains of S.aureus have been reported to cause a numberof diseases or food poisoning outbreaks be-cause of ingestion of contaminated dairy prod-ucts or milk (Adesiyun et al., 1998; Asao et al.,2003; Genigeorgis, 1989). The most recent large-scale outbreak occurred during June 2000 inJapan caused by consumption of low-fat milkproduced from skim milk powder contami-nated with S. aureus enterotoxin A (Asao et al.,2003).

The prevalence of C. jejuni in bulk tank milkhas been reported to range from �1% to slightlymore than 12% (Table 1). Campylobacter jejuni isthe most frequently identified cause of acute in-fectious diarrhea in developed countries, in-cluding the United States (Friedman, 2000).About 2.4–4 million cases of campylobacterio-sis are associated with 120 deaths each year(Mead et al., 1999). Foodborne illness caused byCampylobacter is characterized by sporadic casesof chronic gastritis, enterocolitis, and sep-ticemia. Foodborne infections by Campylobactercan result in sequelae like Campylobacter-associ-ated Guillian-Barré syndrome (Nachamkin,2000). Humans get infected through ingestionof contaminated non-pasteurized milk, milk notproperly pasteurized, untreated water, and rawor improperly cooked poultry (Evans et al.,1996; Fashey et al., 1995; Hanninen et al., 1998;Hutchinson et al., 1995). Campylobacter jejuni areexcreted through feces and animal secretions(Waterman et al., 1984), and dairy cattle get in-fected through ingestion of water and feedscontaminated with manure. Campylobacter jejuniis an infrequent cause of mastitis in dairy cows,and it can be shed in milk of asymptomatic cows(Gundmundson and Chirino-Trejo, 1992). Di-rect milk excretion of C. jejuni by clinicallyhealthy cows has been described and impli-cated in the etiology of human enteritis follow-ing consumption of contaminated milk (Orr etal., 1995). Large-scale outbreaks due to Campy-lobacter have been associated with drinking un-pasteurized milk or contaminated water. Cowmanure is a principal reservoir for Campylobac-ter and farm practices using manure as fertilizeron cropland are considered a risk factor for oc-currence of Campylobacter foodborne disease.

Far less is known about the prevalence ofShiga toxin–producing E. coli (STEC) in milkthan the other major foodborne pathogens.STEC are of immense economic and publichealth significance. STEC O157:H7 is charac-terized by low infectious doses, typically 1–100colony-forming units (Paton and Paton, 1998).STEC are highly pathogenic in humans, wherethey cause serious acute illness and long-termsequelae (Karmali, 1989, 2004; Nataro andKaper, 1998; Paton and Paton, 1998). Manifes-tations of illnesses caused by STEC that arelinked to production of Shiga toxins include,

OLIVER ET AL.118

non-bloody diarrhea, diarrhea-associated hem-orrhagic colitis, hemolytic uremic syndrome(HUS), and thrombotic thrombocytopenic pur-pura (Karmali, 1989). HUS cases in North Amer-ica are predominantly caused by E. coli O157:H7.Enterohemorrhagic E. coli (EHEC) strains consti-tute a subtype of STEC serotypes that have beenfirmly associated with bloody diarrhea and HUS.EHEC are generally more pathogenic than otherSTEC because they possess a fuller complementof virulence determinants that encode produc-tion of intimin and enterohemolysin (Karmali,2004). Serotypes O26, O111, O103, and especiallyO157 have been the predominantly isolatedEHEC (Nataro and Kaper, 1998).

Of the few reports published (Jayarao andHenning, 2001; Murinda et al., 2002b; Steele etal., 1997), the prevalence of STEC in bulk tankmilk has been reported to occur in 0.8–3.8% ofsamples evaluated (Table 1). Murinda et al.(2002b) reported the detection of E. coli O157:H7from eight of 30 (26.7%) dairy farms at differentsampling times. Two of 268 (0.75%) bulk tankmilk samples and eight of 415 (1.93%) culleddairy cow fecal samples tested positive for E. coliO157:H7. Murinda et al. (2004b) isolated O26,O111, O103, and O157:H7 EHEC serotypes fromdairy cows and/or the dairy farm environment.It appears that these serotypes could be of epi-demiological significance in the United States.However, since there are presently no well-de-fined serotype-specific methods for their routineisolation, the epidemiological significance ofnon-O157:H7 STEC or EHEC remains unde-fined.

Reports on the prevalence of STEC associ-ated with mastitis are rare. Stephan and Kuhn(1999) and Barrow and Hill (1989) indicated aprevalence of STEC in E. coli mastitis of 2.75%(four of 145) and 0.5% (one of 237), respectively.Conversely, Cullor (1997) indicated the absenceof Stx-producing E. coli from 500 cases of col-iform mastitis that included E. coli. A recentstudy by Murinda et al. (2004a) demonstratedthat, of 105 E. coli mastitis isolates evaluated,all were stx-negative, suggesting alternativevirulence characteristics are involved in masti-tis; only four of these isolates were positive foreaeA gene sequences. Thus, it would appearthat STEC are rarely associated as a causativeagent of bovine mastitis.

The prevalence of L. monocytogenes in bulktank milk has been reported to range from 1%to �12% (Table 2). Listeria monocytogenes causessepticemia and meningitis in humans. Preg-nant women are particularly susceptible sinceL. monocytogenes infection may result in spon-taneous abortions or stillbirth of the fetus. Lis-teria monocytogenes has been isolated frommammals, birds, fish, crustaceans and insects.In addition, L. monocytogenes are widespread innature and live naturally in plants and soil en-vironments. It can grow in a wide range of tem-perature and pH. This adaptability enables L.monocytogenes to grow in refrigerated raw milkand in low quality silage with a pH of �4.5. Athigh bacterial concentrations, L. monocytogenescan survive minimum HTST pasteurization(Bunning et al., 1988). Listeria monocytogenes cancause mastitis in cows, and it can be shed inmilk of asymptomatic cows (Bourry et al., 1995;Jensen et al., 1996; Winter et al., 2004). Humancontamination occurs through consumption ofraw milk, or products manufactured with rawmilk or ingestion of processed food cross-con-taminated with pathogens present in the foodprocessing plant environment (Gravani, 1999).In cattle, L. monocytogenes can cause neurolog-ical disease, abortion, or asymptomatic infec-tions. Healthy, but infected animals, shed Lis-teria in feces and fecal contamination ofpastures or vegetables has been implicated asa source of contamination for humans and ru-minants. Therefore, spreading untreated ma-nure onto pastures and cropland is regarded asa risk factor for L. monocytogenes foodborne dis-ease.

The prevalence of Salmonella species in bulktank milk has been reported to range from �1%to almost 9% (Table 2). Salmonella species havebeen linked with illness in animals and hu-mans, and are one of the most commonly re-ported causes of human foodborne disease(Mead et al., 1999). Salmonella live in the in-testinal tract of various animal species, includ-ing cattle, and therefore represent a majorreservoir for human foodborne disease. Hu-mans are infected, primarily via fecal contam-ination of food products or water; however, di-rect contact with sick animals or humans areadditional sources of contamination, especiallyfor farm families. A high percentage of human

DAIRY FOOD SAFETY 119

salmonellosis occurs through consumption ofraw milk or dairy products manufactured withraw milk (CDC, 2002, 2003).

Several Salmonella serotypes have been iso-lated from clinically ill cattle. Salmonella enter-ica serotype Typhimurium definitive type 104(DT 104) is of particular concern to animal andpublic health agencies due to its multiple an-timicrobial resistance (Besser et al., 2000). In-line milk filters from farms located in central,east, north, and west regions of New York Statewere evaluated to determine the prevalence ofSalmonella in New York dairy herds. Six of 404(1.5%) milk filters were positive for Salmonellaspp. From these isolates, one was confirmed asS. Typhimurium DT 104 (Hassan et al., 2000).In another study conducted on 12 dairy farmsfrom Minnesota, Michigan, New York, andWisconsin where fecal, bulk tank milk, and en-vironmental samples were analyzed for Salmo-nella, it was found that 1.1% of bulk tank milk(n � 91) and 12.6% of in-line milk filter sam-ples (n � 87) were positive for Salmonella spp.(Warnick et al., 2003).

More recently, there has been an increase ininfections caused by Salmonella enterica serotypeNewport (CDC, 2002; Weir et al., 2004). Theseinfections can be severe. An increasing numberof S. Newport isolates have been shown to beresistant to 9 or more antimicrobial agents(Zhao et al., 2003). Risk factors that may be as-sociated with S. Newport infection in humansinclude direct exposure to dairy farms, inges-tion of raw milk and cheese made from unpas-teurized raw milk, and consumption of raw orundercooked ground beef (Gupta et al., 2003).Results of the recent National Animal HealthMonitoring System Dairy 2002 Survey reportedby Van Kessel et al. (2004) indicated that 2.6%of bulk tank milk samples were culture-positivefor Salmonella, and four of 22 isolates were S.Newport.

PREVALENCE OF FOODBORNEPATHOGENS IN THE DAIRY

ENVIRONMENT

Dairy farms are an important reservoir offoodborne pathogens. The presence of foodbornepathogens in milk is due to direct contact with

contaminated sources in the dairy farm envi-ronment and to excretion from the udder of aninfected animal (Figs. 1 and 2). Most foodbornepathogens inhabit the ruminant intestinal tract,and therefore, dairy cattle are considered a ma-jor reservoir of Salmonella, Campylobacter, andSTEC. Listeria species are widespread in natureand live naturally in plants and soil environ-ments. Epidemiological studies have shown thatcattle probably become infected through con-sumption of water and feedstuffs contaminatedwith feces and other cattle secretions/excretions.Presence of foodborne pathogens in bulk tankmilk seems to be directly linked to fecal conta-mination that occurs primarily during the har-vesting of raw milk, however, some foodbornepathogens can cause mastitis in which case theorganism can be directly excreted into milk. In-troduction of raw milk contaminated with food-borne pathogens into processing plants and theirpersistence in biofilms represents an importantrisk of post-pasteurization contamination thatcould lead to exposure of the consumer to path-ogenic bacteria. (Arizcun et al., 1998; Roberts andWiedmann, 2003; Wong, 1998).

The microaerophilic and thermophilic natureof C. jejuni hampers growth of this organism infeed and in nature. In spite of the fastidious re-quirements of C. jejuni, they are very versatileand metabolically active organisms capable ofexploiting a variety of environments, especiallythe intestinal tract of mammals and birds. Enu-

OLIVER ET AL.120

FIG. 1. Maintenance and recycling of foodborne path-ogens on the dairy farm. Foodborne pathogens originatefrom direct contact with contaminated sources, primarilyfeces, in the dairy farm environment. The primary sourceof foodborne pathogens in milk appears to be directlylinked to fecal contamination that occurs during the milk-ing process.

meration studies have shown that a critical am-plification stage in the Campylobacter cell cycleoccurs in the intestines of asymptomatic ani-mals. Once cells are excreted to the environ-ment, they must utilize survival strategies un-til ingested by a susceptible host. Thus, theintestinal tract and feces of susceptible animals(carriers) are considered the major reservoir ofthis foodborne pathogen. A similar process wasdescribed for L. monocytogenes. Data reportedby Nightingale et al. (2004) supports the modelin which the presence of the pathogen dependson the ingestion of contaminated feed followedby amplification in bovine hosts and fecal dis-semination in the farm environment. A similar

series of events seems to occur with STEC. Theinfluence of the diet (grains vs. forage) on theshedding of STEC in feces suggests that an am-plification stage also occurs in the gastroin-testinal (GI) tract of ruminants. The terminalrectum of the GI tract is an important site wherethis pathogen showed specific tropism (Nayloret al., 2003). Escherichia coli O157:H7 was de-tected in the terminal rectum regardless ofwhether animals were experimentally or natu-rally infected. The pathogen was detected in fe-ces up to 4 weeks after experimental inocula-tion or 22 days in those that cohabited withinfected animals. These findings lead authorsto propose the existence of “super-shedders”

DAIRY FOOD SAFETY 121

FIG. 2. Cycling of foodborne and veterinary pathogens in the dairy farm environment and their transfer to milk.(A) Amplification of the pathogen in the cow. (B) Dissemination in the immediate environment of the cow via feces.(C) Accumulation of feces on the dairy. (D) Spreading cow manure onto croplands. (E) Crops become contaminatedwith pathogens. (F) Contaminated feed consumed by cows. (G) Milk can become contaminated with pathogens dur-ing milking. (H) Pathogens enter bulk tank milk. (I,J) Unpasteurized milk, cheese, and other dairy products madefrom unpasteurized milk consumed by humans.

and colonization of the terminal rectum was apre-condition for this status (Naylor et al.,2003). Taken together, colonization in thebovine GI tract and amplification of C. jejuni,L. monocytogenes and E. coli O157:H7 appear tobe required stages in the cell cycles. Sheddingof foodborne pathogens in feces and distribu-tion in the environment where cows live en-sures animal re-infection and persistence of thepathogen on the farm. This coupled with in-fection of other mammals, birds, and insectsthat live on the farm demonstrate that produc-tion units are a major reservoirs for foodbornepathogens.

A recent study by Murinda et al. (2004b) wasconducted to investigate the major habitats ofpathogens on dairy farms that could act asreservoirs and transient carriers of Salmonellaspp., L. monocytogenes, C. jejuni, and O157 andnon-O157 STEC. Campylobacter jejuni, Salmonellaspp. and L. monocytogenes, sorbitol-negative(SN)–STEC O157:H7 and sorbitol-positive (SP)-STEC, respectively, were isolated from 5.1%,3.8%, 6.5%, 0.7%, and 17.3% of samples evalu-ated. Diverse serotypes of SP-STEC includingO157:H7, O26:H11, O111, and O103 were iso-lated. None of the five pathogen groups stud-ied were isolated from bulk tank milk. Mostfoodborne pathogens (44.2%) were isolated di-rectly from fecal samples. Bovine fecal samples,lagoon water, bedding, bird droppings and ratsconstituted areas of major concern on dairyfarms. Although in-line milk filters from twofarms tested positive for Salmonella or L. mono-cytogenes, none of the pathogens were detectedin the corresponding bulk tank milk samples,probably due to a dilution effect. In anotherstudy conducted on 12 dairy farms from Min-nesota, Michigan, New York, and Wisconsin(Warnick et al., 2003), Salmonella spp. were iso-lated from the sick cow pen floor, calving penfloor, milking cow feed bunk, lagoon or othermanure storage areas, and cow water tank ordrinking cups. From 4049 fecal samples tested,9.3% were Salmonella-positive. The percentageof positive samples per farm ranged from 0.3 to28%. From 811 environmental samples, 12.9%were positive for Salmonella spp. with a rangefrom 0% to 40% per farm.

STEC O157:H7 serotype has been isolatedfrequently from cattle feces, and most human

EHEC O157:H7 infections originate, either di-rectly or indirectly, from this source (Besser etal., 1997, 2001). Several investigations aimed atthe identification of possible interventionstrategies to control the prevalence of E. coliO157:H7 on farms have linked productionpractices (critical points) with persistence ofthis foodborne pathogen in cattle and genera-tion of reservoirs in the farm environment (El-der et al., 2000; Garber et al., 1995; Hancock etal., 1997; Shere et al., 1998; Zhao et al., 1995).Among these, diet (Buchko et al., 2000; Cray etal., 1998; Diez-Gonzalez et al., 1998; Herriot etal., 1998), age of cattle (Cray and Moon, 1995;Garber et al., 1995), management of manureand fecal slurry, contaminated animal drinkingwater (Faith et al., 1996; LeJune et al. 2001;Shere et al., 1998), and management of pre- andpost-weaned calves (Faith et al., 1996; Garberet al., 1995; Shere et al., 1998) have been iden-tified as risk factors for infection and sheddingof E. coli O157:H7 by cattle.

Especially important is the use of manure asa fertilizer or contaminated water to irrigatefield crops. Contaminated manure and irriga-tion water were probable vehicles for thepathogen in many human disease outbreaks.Supporting data was obtained from a studywhere the occurrence and persistence of E. coliO157:H7 was determined on lettuce and pars-ley grown in soil fertilized with contaminatedpoultry or bovine manure composts or treatedwith contaminated irrigation water. Resultsfrom this study indicated that E. coli O157:H7could persist for 154–217 days in soils fertilizedwith contaminated composts. After seedlingswere planted, E. coli O157:H7 could be detectedon lettuce and parsley for up to 77 and 177days, respectively. In addition, E. coli O157:H7persisted in soil for more than 5 months afterapplication of contaminated compost or irriga-tion water, regardless of source or crop type(Islam et al., 2004).

FOOD SAFETY AND PUBLIC HEALTH IMPLICATIONS

Pasteurization is regarded as an effectivemethod for eliminating foodborne pathogensand other bacteria from milk. However, the in-

OLIVER ET AL.122

creasing number of reports on detection of food-borne pathogens in pasteurized fluid milk andready-to-eat dairy products clearly indicatesthat pasteurization alone is not the final solutionfor the control of milkborne pathogens. In ad-dition, consumption of raw milk has been rec-ognized as a major cause of foodborne diseases.Although the true incidence of milkborne dis-ease in the United States is unknown, there arereports that link consumption of contaminatedraw milk, inadequately pasteurized milk, orconsumption of dairy products adulterated withcontaminated raw milk to cases of human food-borne disease (Evans et al., 1996; Fahey et al.,1995; Fleming et al., 1985). For example, a highproportion of human infections caused by C. je-juni occurred through ingestion of untreatedwater, non-pasteurized milk, and inadequatelypasteurized milk contaminated with this food-borne pathogen (Evans et al., 1996; Fahey et al.,1995). Raw milk is also used to produce hardcheeses that are aged for more than 60 days suchas Cheddar, Colby, Parmigiano, and Provolone.Eleven foodborne disease outbreaks associatedwith cheese were reported in the United Statesfrom 1958 to 1991 (CDC, 1996; Johnson et al.,1990). Causative factors in cheese-related dis-ease outbreaks were post-pasteurization conta-mination, faulty pasteurization equipment orprocedures, and use of raw unpasteurized milk(Johnson et al., 1990).

Outbreaks of human salmonellosis have alsobeen linked to ingestion of raw milk contami-nated with Salmonella (CDC, 2003). The 2002–2003 multistate (Illinois, Indiana, Ohio, andTennessee) outbreak of Salmonella Serotype Ty-phimurium infections was linked to an Ohiofarm comprised of a working dairy, restaurant,snack bar, and petting zoo with goats, cows,calves, lambs, and pigs. The dairy was the onlyplace in Ohio that legally sold raw milk in jugs,and served both milk and milk shakes madewith raw milk to customers.

Although numerous studies have docu-mented that foodborne pathogens of publichealth significance have been isolated frombulk tank milk and are capable of causing dis-ease in humans, people continue to consumeraw milk. Many farm families consume rawmilk simply because it is a traditional practiceand it is less expensive to take milk from the

bulk tank than buying pasteurized retail milk.Additionally, some believe that raw milk has ahigher nutritional value than pasteurized milk(Hegarty et al., 2002). A study by Headrick etal. (1997) showed that people with less than ahigh school education were more likely to con-sume raw milk than those who had completedhigh school, suggesting that level of educationmay influence a person’s choice to consumeraw milk.

Rohrbach et al. (1992) reported that 68 of 195(34.9%) dairy producers in East Tennessee andSouthwest Virginia consumed raw bulk tankmilk produced on their farm. Of the bulk tanksfrom which raw milk was consumed by dairyproducers, 25% (17 of 68) contained one ormore species of L. monocytogenes, C. jejuni, Y.enterocolitica and Salmonella (Rohrbach et al.,1992). On farms where producers did not con-sume raw milk, 32% (40 of 127) of bulk tankswere contaminated with one or more of theabove zoonotic pathogens, and bulk tank milkquality was not significantly different fromthose dairy producers who reported that theyconsumed raw milk from the bulk tank (25%,17 of 68). The prevalence of consumption ofbulk tank milk containing one or more poten-tial human pathogenic bacteria among all dairyproducers was 17/195 or 8.7%. Jayarao andHenning (2001) reported that 79 of 131 (60%)dairy producers in eastern South Dakota andwestern Minnesota consumed raw bulk tankmilk produced on their farm. Of the 79 dairyproducers who consumed raw milk, 21 (26.6)contained one or more species of L. monocyto-genes, C. jejuni, Y. enterocolitica, STEC, and Sal-monella. There was no significant difference inthe incidence of pathogenic bacteria in rawmilk of dairy producers who did and did notconsume raw milk. Thus, based on the limitedinformation available, it would appear that nu-merous persons in the rural community con-sume raw unpasteurized bulk tank milk. Usingdata on incidence of raw milk consumption of60% by dairy producers from the survey con-ducted by Jayarao and Henning (2001), and as-suming that 25% of bulk tanks contain one ormore potential human pathogens based ondata reported by Rohrbach et al. (1992) and Ja-yarao and Henning (2001), the prevalence ofconsumption of contaminated bulk tank milk

DAIRY FOOD SAFETY 123

would be 15%. Thus, risk exposure of peoplein the rural community to potential pathogenicbacteria capable of causing disease in humansvia consumption of raw unpasteurized milkcan be very high. Data clearly demonstrate thatconsumption of raw milk increases the chancesof direct contact with foodborne pathogens ortoxins produced by foodborne pathogens (i.e.,S. aureus enterotoxins) and is therefore a riskfactor of human foodborne disease. Educa-tional efforts should be aimed at making therural population aware of the health risks as-sociated with consumption of raw unpasteur-ized milk.

In addition to direct consumption of contam-inated raw milk, introduction of raw milk con-taminated with foodborne pathogens into dairyprocessing plants represents an important riskof contamination of milk products that couldlead to exposure of consumers to pathogenicbacteria. Although milk pasteurization is re-garded as an effective method to eliminate food-borne pathogens, some dairy products do notundergo pasteurization (i.e., specialty cheeses).Furthermore, pathogens such as L. monocyto-genes survive and thrive in post-pasteurizationprocessing environments thus leading to recon-tamination of dairy products. These two signif-icant exposure pathways pose a risk to the con-sumer from direct exposure to foodbornepathogens in unpasteurized dairy products aswell as dairy products that are re-contaminatedin the post-pasteurization processing environ-ment. The increasing number of incidences inwhich foodborne pathogens are detected in fluidmilk and ready-to-eat dairy products clearly in-dicate that pasteurization is not the ultimate toolto control milkborne pathogens. It is likely thatfecal and foodborne pathogen contamination oc-curs during the harvesting of raw milk (i.e.,milking, collection, and storage) and the farmenvironment likely plays a major role in thepresence of foodborne pathogens in bulk tankmilk. Reducing the potential for contaminationduring harvesting of milk should result in a re-duction of foodborne pathogens in raw milk.

Introduction of L. monocytogenes into foodprocessing plants results in reservoirs that aredifficult to eradicate. Biofilms are a constant is-sue in food processing environments. Listeriamonocytogenes survived for extended periods

on stainless steel and rubber, materials com-monly used in food-processing equipment.Some components in the rubber inhibitedgrowth of the organism, but also affected theefficacy of sanitizers on biofilm inactivation.These conditions led to the persistence of lownumbers of L. monocytogenes on equipment surfaces making eradication difficult (Wong,1998). The level of contamination of milk pro-cessing plants was investigated by several re-search groups. In a survey conducted in 39frozen milk plants in California, L. monocyto-genes was the only species recovered from five(12.8%) plants. Observations of this study in-dicated that the type of product received andtype of pasteurization did not influence recov-ery of Listeria from a plant. However, a signif-icant association with size of the plant and re-covery of Listeria was observed. Also, it wasobserved that the level of sanitation and extentof environmental contamination control pro-gram (ECCP) were not associated with recov-ery of Listeria from a plant. The rate of recov-ery of Listeria from plants with above averagesanitation and excellent or moderate ECCP was6.81%, whereas the recovery rate from plantswith below average sanitation and slight or noECCP was 27.5%. Interestingly, the highest re-covery rates of Listeria in frozen milk productplants were in batch flavoring, freezing and in-gredient blending, and package filling areas(Walker et al., 1991). In a study conducted in21 dairy processing plants in Vermont, 80 of378 sites (21.2%) were identified as Listeria-pos-itive, and of these 35 (43.8%) were positive forL. monocytogenes (Pritchard et al., 1995).

Mycobacterium avium subsp. paratuberculosis(MPTB), the etiologic agent of Johne’s diseasein dairy and beef cattle and sheep, is consid-ered by some to be an emerging foodbornepathogen. This concern is based on reports thathave shown that Crohn’s disease in human pa-tients bears a clinical resemblance to Johne’sdisease. Current evidence neither supports orrefutes a mycobacterial cause of Crohn’s dis-ease, but evidence does suggest that either asubset of human patients are presumably in-fected with MPTB or that the ulcerated tissuesof Crohn’s disease patients selectively harborMPTB acquired as an environmental contami-nant or opportunistic pathogen (Bannantine et

OLIVER ET AL.124

al., 2004; Harris and Barletta, 2001; Sechi et al.,2001). Milk from dairy cows with Johne’s dis-ease could be a potential vector in the trans-mission of MPTB to humans based on evidencedemonstrating that the pathogen can be shedand isolated from raw milk and that MPTB maysurvive pasteurization (Grant et al. 2002a,b;Millar et al., 1996).

While the role of MPTB is firmly establishedin Johne’s disease in cattle and sheep, its rolein Crohn’s disease is less clear (Bannantine etal., 2004). The need for a definitive answer tothis important question has been recognized bythe scientific community and is currently beinginvestigated by several research groups. The bi-ology of MPTB makes its manipulation in thelaboratory and development of rapid and accurate diagnostic methods difficult. New de-tection methods are needed to definitively an-swer questions surrounding MPTB as a food-borne pathogen and if this pathogen is acontributing factor in Crohn’s disease. Recentadvances in the study of the MPTB genome andimmunology have led to the identification ofspecific DNA sequences and protein antigensthat may allow reliable detection of MPTB(Bannantine et al., 2004). Improving the detec-tion of MPTB would help to answer funda-mental questions on the epidemiology andpathogenesis of MPTB including its role infoodborne illness.

CONCLUSION

Milk can harbor a variety of microorganismsand can be an important source of foodbornepathogens. The presence of foodborne pathogensin milk can be due to direct contact with conta-minated sources in the dairy farm environmentand to excretion from the udder of an infectedanimal. The dairy industry should be concernedabout dairy food safety because (1) outbreaks ofdisease in humans have been traced to the con-sumption of unpasteurized milk and have alsobeen traced back to pasteurized milk, (2) unpas-teurized milk is consumed directly by dairy pro-ducers and their families, farm employees andtheir families, neighbors, and raw milk advo-cates, (3) unpasteurized milk is consumed di-rectly by a large segment of the population via

consumption of several types of cheeses manu-factured from unpasteurized milk, (4) entry offoodborne pathogens via contaminated raw milkinto dairy food processing plants can lead to per-sistence of these pathogens in biofilms, and sub-sequent contamination of processed milk prod-ucts and exposure of consumers to pathogenicbacteria, (5) pasteurization may not destroy allfoodborne pathogens in milk, and (6) faulty pasteurization will not destroy all foodbornepathogens.

Information presented in this review sup-ports the model in which the presence ofpathogens depends on ingestion of contami-nated feed followed by amplification in bovinehosts and fecal dissemination in the farm en-vironment (Figs. 1 and 2). The final outcome ofthis cycle is a constantly maintained reservoirof foodborne pathogens that can reach the hu-man population by direct contact, ingestion ofraw contaminated food (raw milk or cheesemade with raw milk), or contamination duringthe processing of milk. Isolation of bacterialpathogens with similar biotypes from dairyfarms and from outbreaks of human diseasesubstantiates this hypothesis.

The challenges to providing a safe and nu-tritious food supply are complex because all as-pects of food production—from farm to fork—need to be considered. Given the considerablenational/international demand and expecta-tions for food safety and the formidable chal-lenges of producing and maintaining a safefood supply, food safety research and educa-tional programs has taken on a new urgency.As the system of food production and distrib-ution changes, the food safety system needs to change with it. A strong science-based ap-proach that addresses all the complex issues in-volved in continuing to improve food safetyand public health is necessary to prevent food-borne illnesses. Not only must research be con-ducted to solve complex food safety issues, butalso results of that research must be communi-cated effectively to producers and consumers.Research and educational efforts identifyingpotential on-farm risk factors will better enabledairy producers to reduce/prevent foodbornepathogen contamination of dairy productsleaving the farm. Identification of on-farmreservoirs could aid with implementation of

DAIRY FOOD SAFETY 125

farm-specific pathogen reduction programs.Foodborne pathogens, mastitis, milk qualityand dairy food safety are indeed all interre-lated. A safe, abundant and nutritious milk andmeat supply should be the goal of every dairyproducer in the world.

ACKNOWLEDGMENTS

This work was supported by the Universityof Tennessee Food Safety Center of Excellence,the Tennessee Agricultural Experiment Station,and The University of Tennessee College ofVeterinary Medicine Center of Excellence Re-search Program in Livestock Diseases and Hu-man Health. Authors express their apprecia-tion to personnel in the Lactation/Mastitis/Food Safety Research Program at The Univer-sity of Tennessee for excellent technical assis-tance.

REFERENCES

Adesiyun, A.A., L.A. Webb, and H.T. Romain. 1998.Prevalence and characteristics of Staphylococcus aureusstrains isolated from bulk and composite milk and cattlehandlers. J. Food Prot. 61:629–632.

Arizcun, C., C. Vasseur, and J.C. Labadie. 1998. Effect ofseveral decontamination procedures on Listeria monocyto-genes growing in biofilms. J. Food Prot. 61:731–734.

Asao, T., Y. Kumeda, T. Kawai, et al. 2003. An extensiveoutbreak of staphylococcal food poisoning due to low-fatmilk in Japan: estimation of enterotoxin A in the incrim-inated milk and powdered skim milk. Epidemiol. Infect.130:33–40.

Bannantine, J.P., R.G. Barletta, J.R. Stabel, et al. 2004. Ap-plication of the genome sequence to address concerns thatMycobacterium avium subspecies paratuberculosis might bea foodborne pathogen. Foodborne Path. Dis. 1:3–26.

Barrow, P.A., and A.W. Hill. 1989. The virulence charac-teristics of strains of Escherichia coli isolated from cases ofbovine mastitis in England and Wales. Vet. Microbiol.20:35–48.

Bennet, R. W., M. Yeterian, W. Smith, et al. 1986. Staphy-lococcus aureus identification and enterotoxigenicity. J.Food Sci. 51:1337–1339.

Besser, T.E., D.D. Hancock, L.C. Pritchett, et al. 1997. Du-ration of detection of fecal excretion of Escherichia coliO157:H7 in cattle. J. Infect. Dis. 175:726–729.

Besser, T.E., M. Goldoft, L.C. Pritchett, et al. 2000. Mul-

tiresistant Salmonella Typhimurium DT104 infections ofhumans and domestic animals in the Pacific Northwestof the United States. Epidemiol. Infect. 124:193–2000.

Besser, T.E., B.L. Richards, D.H. Rice, et al. 2001. Es-cherichia coli O157:H7 infection of calves: infectious doseand direct contact transmission. Epidemiol. Infect. 127:555–560.

Bourry, A., B. Poutrel, and J. Rocourt. 1995. Bovine mas-titis caused by Listeria monocytogenes: characteristics ofnatural and experimental infections. J. Med. Microbiol.43:125–132.

Buchko, S.J., R.A. Holley, W.O. Olson, et al. 2000. The ef-fect of fasting and diet on fecal shedding of Escherichia coliO157:H7 by cattle. Can. J. Anim. Sci. 80:741–746.

Bunning, V.K., C.W. Donnelly, J.T. Peeler, et al. 1988.Thermal inactivation of Listeria monocytogenes withinbovine milk phagocytes. Appl. Environ. Microbiol.54:364–370.

Castro, R., R. Schoebitz, L. Montes, et al. 1986. Entero-toxigencity of Staphylococcus aureus strains isolated fromcheese made from unpasteurized milk. Lebensm.-Wiss. U.Technol. 19:401.

Centers for Disease Control and Prevention. 1996. Sur-veillance for foodborne-disease outbreaks in the UnitedStates, 1988–1992. MMWR 45:1.

Centers for Disease Control and Prevention. 2002. Out-break of multi-drug resistant Salmonella Newport-UnitedStates, January–April 2002. MMWR 51:545.

Centers for Disease Control and Prevention. 2003. Multi-state outbreak of Salmonella serotype Typhimurium in-fections associated with drinking unpasteurized milk—Illinois, Indiana, Ohio, and Tennessee, 2002–2003. MMWR52:613.

Centers for Disease Control and Prevention. 2004. Prelim-inary FoodNet data on the incidence of infection withpathogens transmitted commonly through food—selectedsites, United States, 2003. MMWR 53:338.

Cray, W.C., Jr., T.A. Casey, B.T. Bosworth, et al. 1998. Ef-fect of dietary stress on fecal shedding of Escherichia coliO157:H7 in calves. Appl. Environ. Microbiol. 64:1975–1979.

Cray, W.C., Jr., and H.W. Moon. 1995. Experimental in-fection of calves and adult cattle with Escherichia coliO157:H7. Appl. Environ. Microbiol. 61:1586–1590.

Cullor, J.S. 1997. Risks and prevention of contaminationof dairy products. Rev. Sci. Tech. Int. Epiz. 16:472–481.

Davidson, R.J., D.W. Sprung, C.E. Park, et al. 1989. Oc-currence of Listeria monocytogenes, Campylobacter spp., andYersinia enterocolitica in Manitoba raw milk. Can. Inst.Food Sci. Technol. J. 22:70–74.

Diez-Gonzalez, F., T.R. Callaway, M.G. Kizoulis, et al.1998. Grain feeding and the dissemination of acid-resis-tant Escherichia coli from cattle. Science 281:1666–1668.

OLIVER ET AL.126

Doyle, M.P., and D.J. Roman. 1982. Prevalence and sur-vival of Campylobacter jejuni in unpasteurized milk. Appl.Environ. Microbiol. 44:1154–1158.

Elder, R.O., J.E. Keen, G.R. Siragusa, et al. 2000. Correla-tion of enterohemorrhagic Escherichia coli O157 prevalencein feces, hides, and carcasses of beef cattle during pro-cessing. Proc. Natl. Acad. Sci. USA 97:2999–3003.

Evans, M.R., R.J. Roberts, C.D. Ribeiro, et al. 1996. A milk-borne campylobacter outbreak following an educationalfarm visit. Epidemiol. Infect. 117:457–462.

Fahey, T., D. Morgan, C. Gunneburg, et al. 1995. An out-break of Campylobacter jejuni enteritis associated withfailed milk pasteurization. J. Infect. 31:137–143.

Faith, N.G., J.A. Shere, R. Brosch, et al. 1996. Prevalence andclonal nature of Escherichia coli O157:H7 on dairy farms inWisconsin. Appl. Environ. Microbiol. 62:1519–1525.

Farber, J.M., G.W. Sander, and S.A. Malcolm. 1988. Thepresence of Listeria spp. in raw milk in Ontario. Can. J.Microbiol. 34:95–100.

Fedio, W.M., and H. Jackson. 1990. Incidence of Listeriamonocytogenes in raw milk in Alberta. Can. Inst. Food Sci.Technol. J. 23:236–238.

Fleming, D.W., S.L. Cochi, K.L. MacDonald, et al. 1985.Pasteurized milk as a vehicle of infection in an outbreakof listeriosis. N. Engl. J. Med. 312:404–407.

Friedman, C.R., J. Neimann, H.C. Wegener, et al. 2000.Epidemiology of Campylobacter jenuni infections in theUnited States and other industrialized nations. In: Campy-lobacter, 2nd ed. Nachamkin, I., and M.J. Blaser (ed.),American Society for Microbiology Press, Washington,D.C., pp. 121–138.

Garber, L.P., S.J. Wells, D.D. Hancock, et al. 1995. Riskfactors for fecal shedding of Escherichia coli O157:H7 indairy cattle. J. Am. Vet. Med. Assoc. 207:46–49.

Genigeorgis, C.A. 1989. Present state of knowledge onstaphylococcal intoxication. Int. J. Microbiol. 9:327–360.

Grant, I.R., H.J. Ball, and M.T. Rowe. 2002a. Incidence ofMycobacterium avium subsp. paratuberculosis in bulk rawand commercially pasteurized cows’ milk from approveddairy processing establishments in the United Kingdom.Appl. Environ. Microbiol. 68:2428–2435.

Grant, I.R., E.I. Hutchings, and A. McCartney. 2002b. Ef-fect of commercial-scale high-temperature, short-timepasteurization on the viability of Mycobacterium aviumsubsp. paratuberculosis in naturally infected cows’ milk.Appl. Environ. Microbiol. 68:602–607.

Gravani, R. 1999. Incidence and control of Listeria in food-processing facilities. In: Listeria, listeriosis and food safety,2nd ed. Ryser, E.T., and E.H. Marth (ed.), Marcel Decker,New York, pp. 657–709.

Gudmundson, J., and J.M. Chirino-Trejo. 1992. A case ofbovine mastitis caused by Campylobacter jejuni. Zentralbl.Veterinarmed. B 40:326–328.

Gupta, A., J. Fontana, C. Crowe, et al. 2003. Emergence ofmulti-drug resistant Salmonella enterica serotype Newportinfections resistant to expanded-spectrum cephalosporinsin the United States. J. Infect. Dis. 188:1707–1716.

Hancock, D.D., D.H. Rice, L.A. Thomas, et al. 1997. Epi-demiology of Escherichia coli O157:H7 in feedlot cattle. J.Food Prot. 60:462–469.

Hanninen, M.L., M. Niskanen, and L. Korhonen. 1998.Water as a reservoir for Campylobacter jejuni infection incows studied by serotyping and pulsed-field gel elec-trophoresis. Zentralbl. Veterinarmed. B 45:37–42.

Harris, N.B., and R.G. Barletta. 2001. Mycobacterium aviumsubsp. paratuberculosis in veterinary medicine. Clin. Mi-crobiol. Rev. 14:489–512.

Hassan, L., H.O. Mohammed, P.L. McDonough, et al.2000. A cross-sectional study on the prevalence of Liste-ria monocytogenes and Salmonella in New York dairy herds.J. Dairy Sci. 83:2441–2447.

Headrick, M.L., B. Timbo, K.C. Klontz, et al. 1997. Profileof raw milk consumers in California. Public HealthRep.112:418–422.

Hegarty, H., M.B. O’Sullivan, J. Buckley, et al. 2002. Con-tinued raw milk consumption on farms: why? Commun.Dis. Public Health 5:151–156.

Herriott D.E., D.D. Hancock, E.D. Ebel, et al. 1998. Asso-ciation of herd management factors with colonization ofdairy cattle by Shiga-toxin–positive Escherichia coli O157:H7. J. Food Prot. 61:802–807.

Hutchinson, D.N., F.J. Bolton, P.M. Hinchliffe, et al. 1985.Evidence of udder excretion of Campylobacter jejuni as thecause of milk-borne campylobacter outbreak. J. Hyg.(Lond.) 94:205–215.

Islam, M., M.P. Doyle, S.C. Phatak, et al. 2004. Persistenceof enterohemorrhagic Escherichia coli O157:H7 in soil andon leaf lettuce and parsley grown in fields treated withcontaminated manure composts or irrigation water. J.Food Prot. 67:1365–1370.

Jayarao, B.M., and D.R. Henning. 2001. Prevalence offoodborne pathogens in bulk tank milk. J. Dairy Sci.84:2157–2162.

Jensen, N.E., F.M. Aarestrup, J. Jensen, et al. 1996. Liste-ria monocytogenes in bovine mastitis. Possible implicationfor human health. Int. J. Food Microbiol. 32:209–216.

Johnson, E.A., J.H. Nelson, and M. Johnson. 1990. Micro-biological safety of cheese made from heat treated milk.Part I: Executive summary, introduction and history. J.Food Prot. 53:441–452.

Karmali, M.A. 1989. Infection by verocytotoxin-produc-ing Escherichia coli. Clin. Microbiol Rev. 2:223–228.

Karmali, M.A. 2004. Infection by Shiga toxin–producingEscherichia coli: an overview. Mol. Biotechnol. 26:117–122.

Kenny, K., R.F. Reiser, F.D. Bastida-Corcuera, et al. 1993.Production of enterotoxins and toxic shock syndrome

DAIRY FOOD SAFETY 127

toxin in bovine mammary isolates. J. Clin. Microbiol.31:706–707.

LeJeune, J.T., T.E. Besser, and D.D. Hancock. 2001. Cattlewater troughs as reservoirs of Escherichia coli O157. Appl.Environ. Microbiol. 67:3053–3057.

Liewen, M.B., and Plautz, M.W. 1988. Occurrence of Lis-teria monocytogenes in raw milk in Nebraska. J. Food Prot.51:840–841.

Lovett, J., D.W. Francis, and J.M. Hunt. 1983. Isolation ofCampylobacter jejuni from raw milk. Appl. Environ. Mi-crobiol. 46:459–462.

Lovett, J., D.W. Francis, and J.M. Hunt. 1987. Listeria mono-cytogenes in raw milk: detection, incidence, and patho-genicity. J. Food Prot. 50:188–192.

Masud, T., A.M. Ali, and M.A Shah. 1993. Enterotoxi-genicity of Staphylococcus aureus isolated from dairy prod-ucts. Aust. J. Dairy Technol. 48:30–32.

McEwen, S.A., S.W. Martin, R.C. Clarke, et al. 1988. Theprevalence, incidence, geographical distribution, antimi-crobial sensitivity patterns and plasmid profiles of milkfilter Salmonella isolates from Ontario dairy farms. Can. J.Vet. Res. 52:18–22.

McManus, C., and J.M. Lanier. 1987. Salmonella, Campy-lobacter jejuni, and Yersinia enterocolitica in raw milk. J.Food Prot. 50:51–55.

Mead, P.S., L. Slutsker, V. Dietz, et al. 1999. Food-relatedillness and death in the United States. Emerg. Infect. Dis.5:607–625.

Millar, D., J. Ford, and J. Sanderson. 1996. IS900 PCR todetect Mycobacterium paratuberculosis in retail supplies ofwhole pasteurized milk in England and Wales. Appl. En-viron. Microbiol. 62:3446–3452.

Mossel, D.A.A., and P. Van Neten. 1990. Staphylococcusaureus and related Staphylococci in foods: ecology, pro-liferation, toxinogenesis, control and monitoring. J. Appl.Bacteriol. Symp. Suppl. 69:123–145.

Muraoka, W., C. Gay, D. Knowles, et al. 2003. Prevalenceof Listeria monocytogenes subtypes in bulk tank milk of thePacific Northwest. J. Food Prot. 66:1413–1419.

Murinda, S.E., L.T. Nguyen, S.J. Ivey, et al. 2002a. Mole-cular characterization of Salmonella spp. isolated frombulk tank milk and cull dairy cow fecal samples. J. FoodProt. 65:1100–1105.

Murinda, S.E., L.T. Nguyen, S.J. Ivey, et al. 2002b. Preva-lence and molecular characterization of Escherichia coliO157:H7 in bulk tank milk and fecal samples from cullcows: a 12-month survey of dairy farms in east Tennessee.J. Food Prot. 65:752–759.

Murinda, S.E., L.T. Nguyen, T.L. Landers, et al. 2004a.Comparison of Escherichia coli isolates from humans, food,farm and companion animals for presence of Shigatoxin–producing Escherichia coli virulence markers. Food-borne Path. Dis. 1:178–184.

Murinda, S.E., L.T. Nguyen, H.M. Nam, et al. 2004b. De-tection of sorbitol-negative and sorbitol-positive Shigatoxin–producing Escherichia coli, Listeria monocytogenes,Campylobacter jejuni and Salmonella spp. in dairy envi-ronmental samples. Foodborne Path. Dis. 1:97–104.

Nachamkin, I. , B. Mishu Allos, and T.W. Ho. 2000. Campy-lobacter jejuni infections and the association with Guillain-Barré syndrome. In: Nachamkin, I., and M.J. Blaser (ed.),Campylobacter, 2nd ed. American Society for MicrobiologyPress, Washington, D.C., pp. 155–176.

Nataro, J.P., and J.B. Kaper. 1998. Diarrheagenic Es-cherichia coli. Clin. Microbiol. Rev. 11:142–201.

Naylor, S.W., J.C. Low, T.E. Besser, et al. 2003. Lymphoidfollicle-dense mucosa at the terminal rectum is the prin-cipal site of colonization of enterohemorrhagic Escherichiacoli O157:H7 in the bovine host. Infect. Immun. 71:1505–1512.

Nightingale, K.K., Y.H. Schukken, C.R. Nightingale, et al.2004. Ecology and transmission of Listeria monocytogenesinfecting ruminants and in the farm environment. Appl.Environ. Microbiol. 70:4458–4467.

Ombui, J.N., S.M. Arimi, and M. Kayihura. 1992. Rawmilk as a source of enterotoxigenic Staphylococcus aureusand enterotoxins in consumer milk. East Afr. Med. J.69:123–125.

Orr, K.E., N.F. Lightfoot, P.R. Sisson, et al. 1995. Directmilk excretion of Campylobacter jejuni in a dairy cow caus-ing cases of human enteritis. Epidemiol. Infect. 114:15–24.

Paton, J.C., and A.W. Paton. 1998. Pathogenesis and di-agnosis of Shiga toxin–producing Escherichia coli infec-tions. Clin. Microbiol. Rev. 11:450–479.

Pritchard, T.J., K.J. Flanders, and C.W. Donnelly. 1995.Comparison of the incidence of Listeria on equipment ver-sus environmental sites within dairy processing plants.Int. J. Food Microbiol. 26:375–384.

Roberts, A.J., and M. Wiedmann. 2003. Pathogen, host andenvironmental factors contributing to the pathogenesis oflisteriosis. Cell. Mol. Life Sci. 60:904–918.

Rohrbach, B.W., F.A. Draughon, P.M. Davidson, et al.1992. Prevalence of Listeria monocytogenes, Campylobacterjejuni, Yersinia enterocolitica, and Salmonella in bulk tankmilk: risk factors and risk of human exposure. J. FoodProt. 55:93–97.

Ruzickova, V. 1994. Characteristics of Staphylococcus au-reus isolated from dairy farms. Vet. Med. Czech. 39:37–44.

Sechi, L.A., M. Mura, F. Tanda, et al. 2001. Identificationof Mycobacterium avium subsp. paratuberculosis in biopsyspecimens from patients with Crohn’s disease identifiedby in situ hybridization. J. Clin. Microbiol. 39:4514–4517.

Shere, J.A., K.J. Bartlett, and C.W. Kaspar. 1998. Longitu-dinal study of Escherichia coli O157:H7 dissemination onfour dairy farms in Wisconsin. Appl. Environ. Microbiol.64:1390–1399.

OLIVER ET AL.128

Slade, P.J., D.L. Collins-Thompson, and F. Fletcher. 1988.Incidence of Listeria species in Ontario raw milk. Can. Inst.Food Sci. Technol. J. 21:425–429.

Steele, M.L., W.B. McNab, C. Poppe, et al. 1997. Surveyof Ontario bulk tank milk for foodborne pathogens. J.Food Prot. 60:1341–1346.

Stephan, R., and K. Kuhn. 1999. Prevalence of verotoxin-producing Escherichia coli (VTEC) in bovine coli mastitisand their antibiotic resistance patterns. Zentralbl. Veteri-narmed. B 46:423–427.

Takeuchi, S., K. Ishiguro, M. Ikegami, et al. 1998. Pro-duction of toxic shock syndrome toxin by Staphylococcusaureus isolated from mastitic cow’s milk and farm bulkmilk. Vet. Microbiol. 59:251–258.

Van Kessel, J.A., J.S. Karns, L. Gorski, et al. 2004. Preva-lence of Salmonellae, Listeria monocytogenes and fecal co-liforms in bulk tank milk on U.S. dairies. J. Dairy Sci.87:2822–2830.

Waak, E., W. Tham, and M.L. Danielsson-Tham. 2002.Prevalence of Listeria monocytogenes strains isolated fromraw whole milk in farm bulk tanks and dairy plants re-ceiving tanks. Appl. Environ. Microbiol. 68:3366–3370.

Walker, R.L., L.H. Jensen, H. Kinde, et al. 1991. Environ-mental survey for Listeria species in a frozen milk prod-ucts plant in California. J. Food Prot. 54:178–182.

Warnick, L.D., J.B. Kaneene, P.L. Ruegg, et al. 2003. Eval-uation of herd sampling for Salmonella isolation on mid-

west and northeast U.S. dairy farms. Prev. Vet. Med.60:195–206.

Waterman, S.C., R.W. Park, and A.J. Bramley. 1984. Asearch for the source of Campylobacter jejuni in milk. J.Hyg. (Lond.) 93:333–337.

Weir, E., K. Dore, and A. Currie. 2004. Enhanced surveil-lance for Salmonella Newport. Can. Med. Assoc. J.171:127–128.

Winter, P., F. Schilcher, Z. Bago, et al. 2004. Clinical andhistopathological aspects of naturally occurring mastitiscaused by Listeria monocytogenes in cattle and ewes. J. Vet.Med. B 51:176–179.

Wong, A.C. 1998. Biofilms in food processing environ-ments. J. Dairy Sci. 81:2765–2770.

Zhao, T., M.P. Doyle, J. Shere, et al. 1995. Prevalence ofenterohemorragic Escherichia coli O157:H7 in a survey ofdairy herds. Appl. Environ. Microbiol. 61:1290–1293.

Address reprint requests to:S.P. Oliver, Ph.D.

Food Safety Center of Excellence59 McCord Hall

University of TennesseeKnoxville, TN 37996

E-mail: soliver@utk.edu

DAIRY FOOD SAFETY 129

This article has been cited by:

1. Ruud de BoerOutside Constraints 113-140. [CrossRef]2. Patrizio Tremonte, Luca Tipaldi, Mariantonietta Succi, Gianfranco Pannella, Luisa Falasca, Valeria Capilongo, Raffaele Coppola,

Elena Sorrentino. 2014. Raw milk from vending machines: Effects of boiling, microwave treatment, and refrigeration onmicrobiological quality. Journal of Dairy Science . [CrossRef]

3. Simona Panelli, Eva Brambati, Cesare Bonacina, Maria Feligini. 2014. Updating on the fungal composition in Sardinian sheep'smilk by culture-independent methods. Journal of Dairy Research 1-5. [CrossRef]

4. Lorraine Endersen, Jim O'Mahony, Colin Hill, R. Paul Ross, Olivia McAuliffe, Aidan Coffey. 2014. Phage Therapy in the FoodIndustry. Annual Review of Food Science and Technology 5:1, 327-349. [CrossRef]

5. Jin-Woo Jeon, Jee-Hyun Kim, Jong-Mook Lee, Won-Ho Lee, Do-Young Lee, Se-Hwan Paek. 2014. Rapid immuno-analyticalsystem physically integrated with lens-free CMOS image sensor for food-borne pathogens. Biosensors and Bioelectronics 52,384-390. [CrossRef]

6. Ebrahim Rahimi, Hassan Momtaz, Asma Behzadnia, Zeinab Torki Baghbadorani. 2014. Incidence of Listeria species in bovine,ovine, caprine, camel and water buffalo milk using cultural method and the PCR assay. Asian Pacific Journal of Tropical Disease4:1, 50-53. [CrossRef]

7. Armand Maul. 2014. Heterogeneity: A Major Factor Influencing Microbial Exposure and Risk Assessment. Risk Analysis n/a-n/a. [CrossRef]

8. Carvalho de Azevdo Milka, Barbosa dos Santos Grace, Zocche Fernando, Claudio Horta Maurcio, Silva Dias Francesca, Matiuzzida Costa Mateus. 2014. Microbiological evaluation of raw milk and coalho cheese commercialised in the semi-arid region ofPernambuco, Brazil. African Journal of Microbiology Research 8:3, 222-229. [CrossRef]

9. Y. Motarjemi, G.G. Moy, P.J. Jooste, L.E. AnelichMilk and Dairy Products 83-117. [CrossRef]10. Ashraf M. Ahmed, Tadashi Shimamoto. 2014. Isolation and molecular characterization of Salmonella enterica, Escherichia coli

O157:H7 and Shigella spp. from meat and dairy products in Egypt. International Journal of Food Microbiology 168-169, 57-62.[CrossRef]

11. Ylva Persson, Torben Larsen, Ann-Kristin Nyman. 2014. Variation in udder health indicators at different stages of lactation ingoats with no udder infection. Small Ruminant Research 116:1, 51-56. [CrossRef]

12. P.J. Jooste, L. Anelich, Y. MotarjemiSafety of Food and Beverages: Milk and Dairy Products 285-296. [CrossRef]13. Dariush Shanehbandi, Behzad Baradaran, Saeed Sadigh-Eteghad, Habib Zarredar. 2014. Occurrence of Methicillin Resistant and

Enterotoxigenic Staphylococcus aureus in Traditional Cheeses in the North West of Iran. ISRN Microbiology 2014, 1-5. [CrossRef]14. Yuexia Wang, Pengfei Zhao, Huanling Zhang, Wanyi Chen, Xiaoyu Su, Biao Suo. 2013. A simple and rapid realtime PCR assay

for the detection of Shigella and Escherichia coli species in raw milk. Journal für Verbraucherschutz und Lebensmittelsicherheit 8:4,313-319. [CrossRef]

15. Sarah K. McLean, Louise A. Dunn, Enzo A. Palombo. 2013. Phage Inhibition of Escherichia coli in Ultrahigh-Temperature-Treated and Raw Milk. Foodborne Pathogens and Disease 10:11, 956-962. [Abstract] [Full Text HTML] [Full Text PDF] [FullText PDF with Links]

16. Rosangela Freitas, Maria Aparecida Vasconcelos Paiva Brito, Luís Augusto Nero, Antonio Fernandes de Carvalho. 2013.Microbiological Safety of Minas Frescal Cheese (MFC) and Tracking the Contamination of Escherichia coli and Staphylococcusaureus in MFC Processing. Foodborne Pathogens and Disease 10:11, 951-955. [Abstract] [Full Text HTML] [Full Text PDF][Full Text PDF with Links]

17. Jan Soon, Richard BainesManaging Food Safety Risks in the Beef and Dairy Industries 39-76. [CrossRef]18. A. H. LONGENBERGER, M. P. GRONOSTAJ, G. Y. YEE, L. M. JOHNSON, J. F. LANDO, R. E. VOORHEES, K.

WALLER, A. C. WELTMAN, M. MOLL, S. B. LYSS, B. L. CADWELL, L. M. GLADNEY, S. M. OSTROFF. 2013.Yersinia enterocolitica infections associated with improperly pasteurized milk products: southwest Pennsylvania, March–August,2011. Epidemiology and Infection 1-11. [CrossRef]

19. P.A. Luning, K. Kirezieva, G. Hagelaar, J. Rovira, M. Uyttendaele, L. Jacxsens. 2013. Performance assessment of food safetymanagement systems in animal-based food companies in view of their context characteristics: A European study. Food Control. [CrossRef]

20. Lisa Quigley, Orla O'Sullivan, Catherine Stanton, Tom P. Beresford, R. Paul Ross, Gerald F. Fitzgerald, Paul D. Cotter. 2013.The complex microbiota of raw milk. FEMS Microbiology Reviews 37:5, 664-698. [CrossRef]

21. Ewen C. D. ToddGlobalization and epidemiology of foodborne disease 1-25. [CrossRef]

22. Zehra Nur Yuksekdag, Derya Onal Darilmaz, Yavuz Beyatli. 2013. Dairy propionibacterium strains with potential asbiopreservatives against foodborne pathogens and their tolerance–resistance properties. European Food Research and Technology. [CrossRef]

23. Daniela Manila Bianchi, Antonio Barbaro, Silvia Gallina, Nicoletta Vitale, Laura Chiavacci, Maria Caramelli, Lucia Decastelli.2013. Monitoring of foodborne pathogenic bacteria in vending machine raw milk in Piedmont, Italy. Food Control 32:2, 435-439.[CrossRef]

24. Jo Ann S. Van Kessel, Jeffrey. S. Karns, David R. Wolfgang, Ernest Hovingh. 2013. Regional Distribution of Two Dairy-AssociatedSalmonella enterica Serotypes. Foodborne Pathogens and Disease 10:5, 448-452. [Abstract] [Full Text HTML] [Full Text PDF][Full Text PDF with Links]

25. Wendie L. Claeys, Sabine Cardoen, Georges Daube, Jan De Block, Koen Dewettinck, Katelijne Dierick, Lieven De Zutter, AndréHuyghebaert, Hein Imberechts, Pierre Thiange, Yvan Vandenplas, Lieve Herman. 2013. Raw or heated cow milk consumption:Review of risks and benefits. Food Control 31:1, 251-262. [CrossRef]

26. Mariëlle Bruijnis, Henk Hogeveen, Chris Garforth, Elsbeth Stassen. 2013. Dairy farmers' attitudes and intentions towardsimproving dairy cow foot health. Livestock Science . [CrossRef]

27. Pengbo Ning, Kangkang Guo, Liang Cheng, Lei Xu, Chengcheng Zhang, Hongjie Cui, Yuanyuan Cheng, Rui Xu, Wei Liu,Qizhuang Lv, Weiwei Cao, Yanming Zhang. 2013. Pilot survey of raw whole milk in China for Listeria monocytogenes usingPCR. Food Control 31:1, 176-179. [CrossRef]

28. Grégory Francius, Romain Henry, Jérôme F. L. Duval, Emmanuelle Bruneau, Jenny Merlin, Ahmad Fahs, Nathalie Leblond-Bourget. 2013. Thermo-Regulated Adhesion of the Streptococcus thermophilus Δrgg0182 Strain. Langmuir 130405134538008.[CrossRef]

29. Maria-Adelheid Joris, Karen Verstraete, Koen De Reu, Lieven De Zutter. 2013. Longitudinal Follow-Up of the Persistence andDissemination of EHEC on Cattle Farms in Belgium. Foodborne Pathogens and Disease 10:4, 295-301. [Abstract] [Full TextHTML] [Full Text PDF] [Full Text PDF with Links]

30. M. Gurung, H.M. Nam, M.D. Tamang, M.H. Chae, G.C. Jang, S.C. Jung, S.K. Lim. 2013. Prevalence and antimicrobialsusceptibility of Acinetobacter from raw bulk tank milk in Korea. Journal of Dairy Science 96:4, 1997-2002. [CrossRef]

31. Tatsuro Hagi, Keisuke Sasaki, Hisashi Aso, Masaru Nomura. 2013. Adhesive properties of predominant bacteria in raw cow’smilk to bovine mammary gland epithelial cells. Folia Microbiologica . [CrossRef]

32. R. R. Adgamov, N. F. Timchenko, E. A. Zaitseva, V. I. Pushkareva, D. V. Kolbasov, I. Yu. Egorova, N. M. Pukhovskaya, Yu. S.Musatov, L. I. Ivanov, S. A. Ermolaeva. 2013. Ecological and genetic mechanisms of development of epidemiologically significantstrains of sapronosis causative agents. Biology Bulletin Reviews 3:2, 125-138. [CrossRef]

33. Patricia Munsch-Alatossava, Abdul Ghafar, Tapani Alatossava. 2013. Potential of Nitrogen Gas (N2) Flushing to Extend the ShelfLife of Cold Stored Pasteurised Milk. International Journal of Molecular Sciences 14:3, 5668-5685. [CrossRef]

34. Marjo Ruusunen, Marleena Salonen, Hanna Pulkkinen, Marianne Huuskonen, Sanna Hellström, Joana Revez, Marja-LiisaHänninen, Maria Fredriksson-Ahomaa, Miia Lindström. 2013. Pathogenic Bacteria in Finnish Bulk Tank Milk. FoodbornePathogens and Disease 10:2, 99-106. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

35. Dilecta D’Costa, Saroj N. Bhosle, R. B. Dhuri, S. P. Doijad, K. V. Poharkar, D. R. Kalorey, S. B. Barbuddhe. 2013. Prevalence,Serogroups, Shiga-toxin Genes and Pulsed Field Gel Electrophoresis Analyses of Escherichia coli Isolated from Bovine Milk.Proceedings of the National Academy of Sciences, India Section B: Biological Sciences . [CrossRef]

36. Michael J. DarkMycobacterial Species 337-342. [CrossRef]37. Jean C. Buzby, L. Hannah Gould, Magdalena E. Kendall, Timothy F. Jones, Trisha Robinson, Don P. Blayney. 2013.

Characteristics of Consumers of Unpasteurized Milk in the United States. Journal of Consumer Affairs n/a-n/a. [CrossRef]38. Zhenbo Wei, Jun Wang, Xi Zhang. 2013. Monitoring of quality and storage time of unsealed pasteurized milk by voltammetric

electronic tongue. Electrochimica Acta 88, 231-239. [CrossRef]39. Paige Zaitlin, Johanna Dwyer, Gary R. Gleason. 2013. Mistaken Beliefs and the Facts About Milk and Dairy Foods. Nutrition

Today 48:3, 135-143. [CrossRef]40. M. Maifreni, I. Bartolomeoli, F. Frigo, M. Marino10. Safety issues in the production of cheeses from raw milk and natural starters

151-166. [CrossRef]41. M. Maifreni, I. Bartolomeoli, F. Frigo, M. Marino10. Safety issues in the production of cheeses from raw milk and natural starters

151-166. [CrossRef]42. Masahiro Hayashi, Tatsuya Natori, Sayoko Kubota-Hayashi, Machiko Miyata, Kiyofumi Ohkusu, Keiko Kawamoto, Hisao

Kurazono, Souichi Makino, Takayuki Ezaki. 2013. A New Protocol to Detect Multiple Foodborne Pathogens with PCR Dipstick

DNA Chromatography after a Six-Hour Enrichment Culture in a Broad-Range Food Pathogen Enrichment Broth. BioMedResearch International 2013, 1-10. [CrossRef]

43. T.R. Callaway, R.C. Anderson, T.S. Edrington, K.J. Genovese, R.B. Harvey, T.L. Poole, D.J. NisbetNovel methods for pathogencontrol in livestock pre-harvest: an update 275-304. [CrossRef]

44. D. Fernández, M.E. Sanz, A.E. Parma, N.L. Padola. 2012. Short communication: Characterization of Shiga toxin-producingEscherichia coli isolated from newborn, milk-fed, and growing calves in Argentina. Journal of Dairy Science 95:9, 5340-5343.[CrossRef]

45. Fatine Hadrya, Abdelmoula Elouardi, Doha Benali, Hinde Hami, Abdelmajid Soulaymani, Samira Senouci. 2012. Bacterial Qualityof Informally Marketed Raw Milk in Kenitra City, Morocco. Pakistan Journal of Nutrition 11:8, 760-767. [CrossRef]

46. Dagmar Schoder, Peter Rossmanith, Katrin Glaser, Martin Wagner. 2012. Fluctuation in contamination dynamics of L.monocytogenes in quargel (acid curd cheese) lots recalled during the multinational listeriosis outbreak 2009/2010. InternationalJournal of Food Microbiology 157:3, 326-331. [CrossRef]

47. Ginger M. Shipp, James S. Dickson. 2012. A Longitudinal Study of the Establishment and Proliferation of Enterococcus ona Dairy Farm. Foodborne Pathogens and Disease 9:5, 425-430. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDFwith Links]

48. Federica Giacometti, Andrea Serraino, Guido Finazzi, Paolo Daminelli, Marina N. Losio, Norma Arrigoni, Silvia Piva, DanielaFlorio, Raffaela Riu, Renato G. Zanoni. 2012. Sale of Raw Milk in Northern Italy: Food Safety Implications and Comparisonof Different Analytical Methodologies for Detection of Foodborne Pathogens. Foodborne Pathogens and Disease 9:4, 293-297.[Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

49. M.K. Lawan, F.O. Abdulsalaw, A. Suleiman, T. Aluwong, L.S. Yaqub. 2012. Microbial Assessments of Bulk Milk Before and AfterPasteurization in Two Different Dairy Farms in Zaria, Nigeria. International Journal of Dairy Science 7:4, 103-108. [CrossRef]

50. Maria Angélica Costa Dias, Anderson S. Sant’Ana, Adriano G. Cruz, José de Assis F. Faria, Carlos Augusto Fernandes de Oliveira,Evandro Bona. 2012. On the implementation of good manufacturing practices in a small processing unity of mozzarella cheesein Brazil. Food Control 24:1-2, 199-205. [CrossRef]

51. Sophie Marchand, Jan De Block, Valerie De Jonghe, An Coorevits, Marc Heyndrickx, Lieve Herman. 2012. Biofilm Formationin Milk Production and Processing Environments; Influence on Milk Quality and Safety. Comprehensive Reviews in Food Scienceand Food Safety 11:2, 133-147. [CrossRef]

52. Paulo de Souza Costa Sobrinho, Camila Andreata Marçal de Faria, Julia Silva Pinheiro, Héllen Gonçalves de Almeida, ChristianoVieira Pires, Aline Silva Santos. 2012. Bacteriological Quality of Raw Milk Used for Production of a Brazilian Farmstead RawMilk Cheese. Foodborne Pathogens and Disease 9:2, 138-144. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDFwith Links]

53. Sanna M. Sillankorva, Hugo Oliveira, Joana Azeredo. 2012. Bacteriophages and Their Role in Food Safety. International Journalof Microbiology 2012, 1-13. [CrossRef]

54. Tryness Anastazia Mhone, Gift Matope, Petronella Tapiwa Saidi. 2012. Detection of Salmonella spp., Candida albicans, Aspergillusspp., and Antimicrobial Residues in Raw and Processed Cow Milk from Selected Smallholder Farms of Zimbabwe. VeterinaryMedicine International 2012, 1-5. [CrossRef]

55. I. H. Konosonoka, A. Jemeljanovs, B. Osmane, D. Ikauniece, G. Gulbe. 2012. Incidence of Listeria spp. in Dairy Cows Feed andRaw Milk in Latvia. ISRN Veterinary Science 2012, 1-5. [CrossRef]

56. Jesús Andrei Rosales-Castillo, Ma. Soledad Vázquez-Garcidueñas, Hugo Álvarez-Hernández, Omar Chassin-Noria, Alba IreneVarela-Murillo, María Guadalupe Zavala-Páramo, Horacio Cano-Camacho, Gerardo Vázquez-Marrufo. 2011. Genetic diversityand population structure of Escherichia coli from neighboring small-scale dairy farms. The Journal of Microbiology 49:5, 693-702.[CrossRef]

57. Melisa Anderson, Patrice Hinds, Stacyann Hurditt, Princena Miller, Donovan McGrowder, Ruby Alexander-Lindo. 2011. Themicrobial content of unexpired pasteurized milk from selected supermarkets in a developing country. Asian Pacific Journal ofTropical Biomedicine 1:3, 205-211. [CrossRef]

58. C.J.B. Oliveira, E.R. Hisrich, J.F.P. Moura, P.E.N. Givisiez, R.G.Costa, W.A. Gebreyes. 2011. On farm risk factors associated withgoat milk quality in Northeast Brazil. Small Ruminant Research 98:1-3, 64-69. [CrossRef]

59. Edward M. Fox, Nola Leonard, Kieran Jordan. 2011. Molecular Diversity of Listeria monocytogenes Isolated from Irish DairyFarms. Foodborne Pathogens and Disease 8:5, 635-641. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

60. K. Fotou, A. Tzora, Ch. Voidarou, A. Alexopoulos, S. Plessas, I. Avgeris, E. Bezirtzoglou, K. Akrida-Demertzi, P.G. Demertzis.2011. Isolation of microbial pathogens of subclinical mastitis from raw sheep’s milk of Epirus (Greece) and their role in its hygiene.Anaerobe . [CrossRef]

61. Ryan Newkirk, Craig Hedberg, Jeff Bender. 2011. Establishing a Milkborne Disease Outbreak Profile: Potential Food DefenseImplications. Foodborne Pathogens and Disease 8:3, 433-437. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDFwith Links]

62. Michael Rowe, John DonaghyMicrobiological Aspects of Dairy Ingredients 59-101. [CrossRef]63. K. K. Addo, G. I. Mensah, K. G. Aning, N. Nartey, G. K. Nipah, C. Bonsu, M. L. Akyeh, H. L. Smits. 2011. Microbiological

quality and antibiotic residues in informally marketed raw cow milk within the coastal savannah zone of Ghana. Tropical Medicine& International Health 16:2, 227-232. [CrossRef]

64. M. Walkling-Ribeiro, O. Rodríguez-González, S. Jayaram, M.W. Griffiths. 2011. Microbial inactivation and shelf life comparisonof ‘cold’ hurdle processing with pulsed electric fields and microfiltration, and conventional thermal pasteurisation in skim milk.International Journal of Food Microbiology 144:3, 379-386. [CrossRef]

65. Moustafa El-Shenawy, Mohamed El-Shenawy, Jordi Mañes, Jose M. Soriano. 2011. Listeria spp. in Street-Vended Ready-to-EatFoods. Interdisciplinary Perspectives on Infectious Diseases 2011, 1-6. [CrossRef]

66. T.R. Callaway, T.S. Edrington, R.C. Anderson, J.A. Byrd, M.H. Kogut, R.B. Harvey, D.J. Nisbet, C.W. AielloUsing antimicrobialcultures, bacteriocins and bacteriophages to reduce carriage of foodborne pathogens in cattle and swine 204-224. [CrossRef]

67. J. S. Van Kessel, Y. SchukkenTracing zoonotic pathogens in dairy production 503-526. [CrossRef]68. Åsa Rosengren, Ane Fabricius, Bengt Guss, Susanne Sylvén, Roland Lindqvist. 2010. Occurrence of foodborne pathogens and

characterization of Staphylococcus aureus in cheese produced on farm-dairies. International Journal of Food Microbiology 144:2,263-269. [CrossRef]

69. Tércia M. Ludoulfo de Oliveira, Izabelle S. Rehfeld, Jaqueline Maria Ferreira Siqueira, Jônatas S. Abrahão, Rafael K. Campos,Andréia Kelly R. dos Santos, Mônica Maria O.P. Cerqueira, Erna G. Kroon, Zélia I.P. Lobato. 2010. Vaccinia Virus Is NotInactivated After Thermal Treatment and Cheese Production Using Experimentally Contaminated Milk. Foodborne Pathogensand Disease 7:12, 1491-1496. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

70. Mario Jacques, Virginia Aragon, Yannick D. N. Tremblay. 2010. Biofilm formation in bacterial pathogens of veterinary importance.Animal Health Research Reviews 11:02, 97-121. [CrossRef]

71. PHOTIS PAPADEMAS, THOMAS BINTSIS. 2010. Food safety management systems (FSMS) in the dairy industry: A review.International Journal of Dairy Technology 63:4, 489-503. [CrossRef]

72. Ebrahim Rahimi, Mehrdad Ameri, Hassan Momtaz. 2010. Prevalence and antimicrobial resistance of Listeria species isolatedfrom milk and dairy products in Iran. Food Control 21:11, 1448-1452. [CrossRef]

73. Ana Maria Oliveira, Norma Teruko Nago Miya, Anderson S. Sant’Ana, José Luiz Pereira. 2010. Behavior and EnterotoxinProduction by Coagulase Negative Staphylococcus in Cooked Ham, Reconstituted Skimmed Milk, and Confectionery Cream.Journal of Food Science 75:7, M475-M481. [CrossRef]

74. Maria Kousta, Marios Mataragas, Panagiotis Skandamis, Eleftherios H. Drosinos. 2010. Prevalence and sources of cheesecontamination with pathogens at farm and processing levels. Food Control 21:6, 805-815. [CrossRef]

75. Emiliane Andrade Araújo, Nélio José Andrade, Luis Henrique Mendes Silva, Antônio Fernandes Carvalho, Cleuber Antônio SáSilva, Afonso Mota Ramos. 2010. Control of Microbial Adhesion as a Strategy for Food and Bioprocess Technology. Food andBioprocess Technology 3:3, 321-332. [CrossRef]

76. Sebastien Breurec, Rodrigue Poueme, Cheikh Fall, Adama Tall, Abdoulaye Diawara, Rianatou Bada-Alambedji, Cecile Broutin,Alexandre Leclercq, Benoit Garin. 2010. Microbiological Quality of Milk from Small Processing Units in Senegal. FoodbornePathogens and Disease 7:5, 601-604. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

77. Manuel Simões, Lúcia C. Simões, Maria J. Vieira. 2010. A review of current and emergent biofilm control strategies. LWT -Food Science and Technology 43:4, 573-583. [CrossRef]

78. Ramon Silva, Adriano G. Cruz, José A.F. Faria, Miriam M.L. Moura, Lúcia M.J. Carvalho, Eduardo H.M. Water, Anderson S.Sant'Ana. 2010. Pasteurized Milk: Efficiency of Pasteurization and Its Microbiological Conditions in Brazil. Foodborne Pathogensand Disease 7:2, 217-219. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

79. Maria Beatriz Tassinari Ortolani, Anderson Keizo Yamazi, Paula Mendonça Moraes, Gabriela Nogueira Viçosa, Luís Augusto Nero.2010. Microbiological Quality and Safety of Raw Milk and Soft Cheese and Detection of Autochthonous Lactic Acid Bacteriawith Antagonistic Activity Against Listeria monocytogenes, Salmonella Spp., and Staphylococcus aureus. Foodborne Pathogensand Disease 7:2, 175-180. [Abstract] [Full Text HTML] [Full Text PDF] [Full Text PDF with Links]

80. M.W. GriffithsThe microbiological safety of raw milk 27-63. [CrossRef]81. B. Stessl, I. HeinIdentifying pathogens in milk 87-112. [CrossRef]

82. Kurt J. Boudonck, Matthew W. Mitchell, Jacob Wulff, John A. Ryals. 2009. Characterization of the biochemical variability ofbovine milk using metabolomics. Metabolomics 5:4, 375-386. [CrossRef]

83. Jônatas S. Abrahão, Tércia M.L. Oliveira, Rafael K. Campos, Marieta C. Madureira, Erna G. Kroon, Zélia I.P. Lobato. 2009.Bovine Vaccinia Outbreaks: Detection and Isolation of Vaccinia Virus in Milk Samples. Foodborne Pathogens and Disease 6:9,1141-1146. [Abstract] [Full Text PDF] [Full Text PDF with Links]

84. Stephen P. Oliver, Kathryn J. Boor, Steven C. Murphy, Shelton E. Murinda. 2009. Food Safety Hazards Associated withConsumption of Raw Milk. Foodborne Pathogens and Disease 6:7, 793-806. [Abstract] [Full Text PDF] [Full Text PDF with Links]

85. Enrica Omiccioli, Giulia Amagliani, Giorgio Brandi, Mauro Magnani. 2009. A new platform for Real-Time PCR detection ofSalmonella spp., Listeria monocytogenes and Escherichia coli O157 in milk. Food Microbiology 26:6, 615-622. [CrossRef]

86. N.R. Perkins, D.F. Kelton, K.J. Hand, G. MacNaughton, O. Berke, K.E. Leslie. 2009. An analysis of the relationship between bulktank milk quality and wash water quality on dairy farms in Ontario, Canada. Journal of Dairy Science 92:8, 3714-3722. [CrossRef]

87. Steve Harakeh, Imane Saleh, Omar Zouhairi, Elias Baydoun, Elie Barbour, Nisreen Alwan. 2009. Antimicrobial resistance ofListeria monocytogenes isolated from dairy-based food products. Science of The Total Environment 407:13, 4022-4027. [CrossRef]

88. Cristina Blasco, Yolanda Picó, Vicente Andreu. 2009. Analytical method for simultaneous determination of pesticide and veterinarydrug residues in milk by CE-MS. ELECTROPHORESIS 30:10, 1698-1707. [CrossRef]

89. A.K. Pradhan, J.S. Van Kessel, J.S. Karns, D.R. Wolfgang, E. Hovingh, K.A. Nelen, J.M. Smith, R.H. Whitlock, T. Fyock, S.Ladely. 2009. Dynamics of endemic infectious diseases of animal and human importance on three dairy herds in the northeasternUnited States. Journal of Dairy Science 92:4, 1811-1825. [CrossRef]

90. M. Abraham, P. Venter, J.F.R. Lues, O. de Smidt, I. Ivanov. 2009. Changes in lipopolysaccharide- related endotoxicity of food-borne pathogens in response to safety treatments practised in South Africa. British Food Journal 111:6, 528-538. [CrossRef]

91. Jeffrey T. LeJeune, Päivi J. Rajala‐Schultz. 2009. Unpasteurized Milk: A Continued Public Health Threat. Clinical InfectiousDiseases 48:1, 93-100. [CrossRef]

92. Z.A. Shojaei, A. Yadollahi. 2008. Physicochemical and Microbiological Quality of Raw, Pasteurized and UHT Milks in Shops.Asian Journal of Scientific Research 1:5, 532-538. [CrossRef]

93. F. Pérez-Rodríguez, A. Valero, E. Carrasco, R.M. García, G. Zurera. 2008. Understanding and modelling bacterial transfer tofoods: a review. Trends in Food Science & Technology 19:3, 131-144. [CrossRef]

94. S. Hellström, K. Kiviniemi, T. Autio, H. Korkeala. 2008. Listeria monocytogenes is common in wild birds in Helsinki region andgenotypes are frequently similar with those found along the food chain. Journal of Applied Microbiology 104:3, 883-888. [CrossRef]

95. J SOFOS. 2008. Challenges to meat safety in the 21st century☆. Meat Science 78:1-2, 3-13. [CrossRef]96. M MARCO, M WELLSBENNIK. 2007. Impact of bacterial genomics on determining quality and safety in the dairy production

chain. International Dairy Journal . [CrossRef]97. Efrain Ribot, Eija Hyytia-Trees, Kara CooperPulseNet and Emerging Foodborne Diseases . [CrossRef]98. A ADESIYUN, S STOUTE, B DAVID. 2007. Pre-processed bovine milk quality in Trinidad: Prevalence and characteristics

of bacterial pathogens and occurrence of antimicrobial residues in milk from collection centres. Food Control 18:4, 312-320.[CrossRef]

99. Renata Ivanek, Yrjö T. Gröhn, Martin Wiedmann. 2006. Listeria monocytogenes in Multiple Habitats and Host Populations:Review of Available Data for Mathematical Modeling. Foodborne Pathogens and Disease 3:4, 319-336. [Abstract] [Full Text PDF][Full Text PDF with Links]

100. B.A. Straley, S.C. Donaldson, N.V. Hedge, A.A. Sawant, V. Srinivasan, S.P. Oliver, B.M. Jayarao. 2006. Public Health Significanceof Antimicrobial-Resistant Gram-Negative Bacteria in Raw Bulk Tank Milk. Foodborne Pathogens and Disease 3:3, 222-233.[Abstract] [Full Text PDF] [Full Text PDF with Links]

101. B.M. Jayarao, S.C. Donaldson, B.A. Straley, A.A. Sawant, N.V. Hegde, J.L. Brown. 2006. A Survey of Foodborne Pathogens inBulk Tank Milk and Raw Milk Consumption Among Farm Families in Pennsylvania. Journal of Dairy Science 89:7, 2451-2458.[CrossRef]