J. Dairy Sci. 88:450-465
© American Dairy Science Association, 2005.
Invited Review: Prevalence of Shiga Toxin-Producing Escherichia coli in Dairy Cattle and Their Products
H. S. Hussein and
T. Sakuma
Department of Animal Biotechnology, University of Nevada-Reno, Reno 89557
Corresponding author: H. S. Hussein; e-mail: hhussein{at}cabnr.unr.edu.
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ABSTRACT
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The main objective of this review was to assess the role of dairy cattle and their products in human infections with Shiga toxin-producing Escherichia coli (STEC). A large number of STEC strains (e.g., members of the serogroups O26, O91, O103, O111, O118, O145, and O166) have caused major outbreaks and sporadic cases of human illnesses that have ranged from mild diarrhea to the life-threatening hemolytic uremic syndrome. These illnesses were traced to O157 and non-O157 STEC. In most cases, STEC infection was attributed to consumption of ground beef or dairy products that were contaminated with cattle feces. Thus, dairy cattle are considered reservoirs of STEC and can impose a significant health risk to humans. The global nature of food supply suggests that safety concerns with beef and dairy foods will continue and the challenges facing the dairy industry will increase at the production and processing levels. In this review, published reports on STEC in dairy cattle and their products were evaluated to achieve the following specific objectives: 1) to assemble a database on human infections with STEC from dairy cattle, 2) to assess prevalence of STEC in dairy cattle, and 3) to determine the health risks associated with STEC strains from dairy cattle. The latter objective is critically important, as many dairy STEC isolates are known to be of high virulence. Fecal testing of dairy cattle worldwide showed wide ranges of prevalence rates for O157 (0.2 to 48.8%) and non-O157 STEC (0.4 to 74.0%). Of the 193 STEC serotypes of dairy cattle origin, 24 have been isolated from patients with hemolytic uremic syndrome. Such risks emphasize the importance and the need to develop long-term strategies to assure safety of foods from dairy cattle.
Key Words: foodborne pathogen • Escherichia coli • dairy cattle • Shiga toxin
Abbreviation key: eae = E. coli attaching and effacing gene, ehxA = enterohemolysin gene, HUS = hemolytic uremic syndrome, HUT = an untypeable H antigen, H– = nonmotile, OR = a rough O antigen, OUT = an untypeable O antigen, OX3 = the provisional designation for the O174 antigen, STEC = Shiga toxin-producing E. coli, Stx1 = Shiga toxin 1, stx1 = Shiga toxin 1 gene, Stx2 = Shiga toxin 2, stx2 = Shiga toxin 2 gene.
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INTRODUCTION
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The safety concern about foods of bovine origin emerged 2 decades ago and increased in recent years because of the growing number of human infections with Shiga toxin-producing Escherichia coli (STEC). These infections result in illnesses (Griffin and Tauxe, 1991) such as mild diarrhea, bloody diarrhea, hemorrhagic colitis, and hemolytic uremic syndrome (HUS). Hemolytic uremic syndrome can lead to acute or chronic renal failure, especially in children (Siegler et al., 1991). Other illnesses include strokes (Griffin and Tauxe, 1991) and thrombotic thrombocytopenic purpura that is characterized by nervous system abnormalities (Paton and Paton, 2000).
Dairy cattle are considered reservoirs of O157 (Besser and Hancock, 1994; Hancock et al., 1994; Mechie et al., 1997) and non-O157 STEC (Rahn et al., 1997; Conedera et al., 2001; Kobayashi et al., 2001). Contamination of raw milk (Wells et al., 1991; Sandhu et al., 1996; Chiueh et al., 2002), cheese (Clarke et al., 1994; Pradel et al., 2000; Pradel et al., 2001), or ground beef from dairy cattle (Doyle, 1991) poses a significant risk to humans. Raw milk caused a small number of human illness outbreaks (USDA-APHIS-VS, 1997) that were traced to O157 (Martin et al., 1986; Borczyk et al., 1987; Lahti et al., 2002) and non-O157 STEC (CDC, 1995; Bielaszewska et al., 2000; Allerberger et al., 2001). Outbreaks and sporadic cases of illnesses were also traced to consumption of STEC-contaminated cheese (Deschênes et al., 1996; CDC, 2000) and yogurt (Morgan et al., 1993). Culled dairy cows are mainly used for production of ground beef (USDA-APHIS-VS, 1996a) and therefore can impose a significant health risk (Ostroff et al., 1990; Doyle, 1991; Faith et al., 1996). Because of the increased concern with the safety of ground beef and dairy products in recent years, the objective of this review was to assess the role of dairy cattle in human infections with STEC.
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VIRULENCE FACTORS OF STEC
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In addition to E. coli O157:H7, >100 STEC serotypes (e.g., members of the O26, O91, O103, O111, O118, O145, and O166 serogroups) are known to cause human illnesses, including HUS (Paton and Paton, 2000). Pathogenic STEC strains are often referred to as enterohemorrhagic E. coli and are known to produce 1 or 2 toxins that resemble those of Shigella dysenteriae (O’Brien and Holmes, 1987). These are Shiga toxin 1 (Stx1) and Shiga toxin 2 (Stx2). The STEC strains can also produce other virulence factors such as those responsible for intimate attachment to the intestinal surface (intimin) and for enterocyte damage (enterohemolysin). In addition to E. coli O157:H7, members of the O26, O103, and O111 serogroups are considered the most important enterohemorrhagic E. coli (Franke et al., 1995). Although Stx1 and Stx2 are different proteins, encoded by the Shiga toxin 1 gene (stx1) and the Shiga toxin 2 gene (stx2), respectively, their biological activities are quite similar (Neill, 1997). It is worth noting that STEC-related illnesses can be caused by an E. coli strain that produces Stx1, Stx2, or both toxins (Lior, 1994). Other virulence factors (intimin and enterohemolysin) are encoded by the E. coli attaching and effacing (eae) and enterohemolysin (ehxA) genes. The eae and ehxA genes are found in virtually all E. coli O157 strains (Neill, 1997) and appear to be more common in the non-O157 STEC strains responsible for human illnesses (Beutin et al., 1994). The eae and ehxA genes, however, are not absolutely required to cause human illnesses because STEC strains lacking these genes were shown to cause human illnesses (Neill, 1997). Therefore, each STEC strain should be considered a potential enterohemorrhagic E. coli (Bürk et al., 2002).
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HUMAN INFECTIONS WITH STEC FROM DAIRY CATTLE
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Most human STEC infections have been traced to consumption of contaminated foods of bovine origin such as ground beef (Griffin and Tauxe, 1991; USDA-APHIS-VS, 1997) and raw milk (Herriott et al., 1994; Lahti et al., 2002). Other infection routes include manure-contaminated vegetables (Cieslak et al., 1993), person to person (Reida et al., 1994), animal to person (Crump et al., 2002), and contaminated water through drinking (Yatsuyanagi et al., 2002) or swimming (Keene et al., 1994). Beef from dairy cattle, raw milk, and some of the dairy products are considered contributing factors to STEC infections (Martin et al., 1986; Steele et al., 1997). Shiga toxin-producing E. coli also can spread from the dairy farm environment to humans by touching the animals (Crump et al., 2002). These pathogens were prevalent at high rates on US dairy farms (Zhao et al., 1995) and were widely distributed in the dairy farm environment (Zhao et al., 1995).
Several outbreaks and sporadic cases of human illnesses caused by infection with E. coli O157 (O157:H7, O157:H– [nonmotile], or other isolates that were not typed for the H antigen) from dairy cattle (Table 1
) emphasized the role of raw milk as an important vehicle of transmission (Reitsma and Henning, 1996). With regard to E. coli O157:H7, 2 US outbreaks (Herriott et al., 1994; USDA-APHIS-VS, 1997) were caused by consumption of raw milk in 1992 (9 cases) and 1993 (6 cases) and were traced to 2 dairies that were licensed to sell raw milk (USDA-APHIS-VS, 1994). Drinking raw milk in the US resulted in HUS cases in Wisconsin (Martin et al., 1986), Washington State (Wells et al., 1991), and Oregon (Keene et al., 1997). Raw milk also caused human illnesses in Canada (Borczyk et al., 1987; Wilson et al., 1996) and Finland (Lahti et al., 2002). Fortunately, the number of raw milk drinkers in Western societies is small. It was estimated that 1 to 2% of the US population consume raw milk (USDA-APHIS-VS, 1994). Raw milk consumption, however, has decreased from 429 million kg in 1980 to 230 million kg in 1990 (USDA, 1992). These statistics may explain why the number of STEC outbreaks caused by raw milk consumption has been small.
Outbreaks caused by E. coli O157-contaminated dairy products are limited. For example, the only reported yogurt outbreak occurred in the UK in 1991 (Morgan et al., 1993) and involved 16 people, of which 5 had HUS. Only one cheese outbreak was reported in the US (Wisconsin) and involved 55 people. In addition to the 4 cheese outbreaks that occurred in the UK (Table 1
), 2 cheese outbreaks were also reported in France (Anonymous, 1994) and the UK (Curnow, 1994). Other contaminated dairy products (butter and unpasteurized cream) were the cause of O157 infection in one (Reid, 2001) and 7 (CDSC, 1998) adults, respectively, in the UK.
Although many human illness outbreaks were traced to ground beef (USDA-APHIS-VS, 1997), the beef source (beef or dairy cattle) was not known in most cases. This is because ground beef is produced mainly from culled dairy and beef cattle and includes low-value cuts from finished steers or heifers. Cows culled because of health, age, or production reasons are a significant component of the hamburger consumed in the US; 6 million culled dairy cows enter the food chain as ground beef annually (Troutt and Osburn, 1997; National Cattlemen’s Beef Association, 2001). Culled dairy cows account for 17% of the ground beef produced in the US (Troutt and Osburn, 1997). In New York State alone, culled dairy cows contribute 4.8 million kg of hamburger annually (Segelken, 1996). In general, it is difficult to trace a specific ground beef outbreak to dairy or beef cattle. The only 2 known dairy beef outbreaks are summarized in Table 1.
Contact with dairy farm environments through touching the cattle or their manure resulted in severe cases of E. coli O157:H7-related illnesses (HUS) in the US (Crump et al., 2002; Georgia Division of Public Health, 2002). The illnesses were associated with farm visitors, and no symptoms were reported for farm residents or employees (Crump et al., 2002). Visitors who washed their hands also did not become ill, indicating a protective effect of hand washing. Two severe cases attributable to visiting a dairy farm were also reported in the Czech Republic and were caused by E. coli O157:H– (Bielaszewska et al., 2000). As shown in Table 1, responses to infection varied from no signs of illness (Wilson et al., 1996; Lahti et al., 2002) to bloody diarrhea and HUS (Lahti et al., 2002) and reflected the immunity status of the affected individuals (mostly children). In general, previous exposure to farm animals is known to decrease the risk of infection with STEC (Wilson et al., 1997). In a study of numerous environmental sites on dairy farms (Blanco et al., 2001), evidence of STEC was found in composite samples of calf feeders (19%), calf-barn surfaces (18%), cow feeders (15%), and cow-barn surfaces (11%). Therefore, contaminated farm environments may remain sources of STEC infection for several months.
Infections with non-O157 STEC from dairy cattle are summarized in Table 2. Most of those were traced to consumption of raw milk, as was the case with the US outbreak (CDC, 1995). The remaining raw milk outbreaks occurred in Canada (Wilson et al., 1996) and Germany (Gallien et al., 1997). Although E. coli O5:H– and O103:H2 serotypes were not shown to cause any signs of illness (Table 2), they are known to cause HUS (WHO, 1998). Several outbreaks were also attributed to consumption of cheeses (those made from unpasteurized milk) in Sweden, the UK, the US (Adams and Motarjemi, 1999), and France (Deschênes et al., 1996). Brie cheese was responsible for the outbreaks in Sweden and the US, whereas local cheeses were responsible for the remaining ones. Contact with dairy cattle manure was also the cause of Canadian outbreaks of STEC (O5:H– and O7:H4) infections (Wilson et al., 1996).
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STEC SEROTYPES FROM MILK AND DAIRY PRODUCTS
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Studies on contamination of milk or its products with E. coli, in general, have been limited. Testing raw milk and cheese samples (500 and 739, respectively) revealed low levels (<20 cfu/g) of E. coli contamination (Coia et al., 2001). Detection of STEC in raw milk, milk filters, and cheeses (Table 3) was reported in Canada, Belgium, Germany, the UK, and the US (WHO, 1998). Padhye and Doyle (1991) reported that E. coli O157:H7 was detected in raw milk and cheese. Two STEC serotypes (O91:H21 and an untypeable O antigen [OUT]:H–) and members of the O91 and O113 serogroups were isolated from raw milk and cheese (Table 3). None of these isolates is known to cause human illnesses attributable to the consumption of dairy foods. However, E. coli O91:H21 and OUT:H– were isolated from patients with HUS and bloody diarrhea, respectively (WHO, 1998). Interestingly, the E. coli OUT:H8 found in milk filters (Table 3) is known to cause HUS (Table 2). Of E. coli isolates (O6:H10, O26:H32, O116:H–, and OUT:H–) found in Canadian cheeses (WHO, 1998), 2 serotypes (O26:H32 and OUT:H–) are known to cause HUS (WHO, 1998). Recently, several STEC strains (members of the O8, O103, O156, and O157 serogroups) were isolated from raw milk tanks in the UK (McKee et al., 2003). Although these isolates had 1 (stx1 in O103 and stx2 in O8 and O156) or 2 (stx2 and eae in O157) virulence factors, only members of the O103 and O157 serogroups are known to cause human illnesses (WHO, 1998).
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DAIRY CATTLE AS RESERVOIRS OF STEC
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Although STEC are not host specific, they are more prevalent in ruminants than in other animals (Riemann and Cliver, 1998). In addition, human illnesses caused by STEC infection have been traced mostly to cattle (Dean-Nystrom et al., 1997). Therefore, cattle (Martin et al., 1986; Wilson et al., 1992; Chapman et al., 1993), including dairy cows, heifers, and calves (Hancock et al., 1994; Zhao et al., 1995; Besser et al., 1997), have been considered reservoirs of STEC. Zhao et al. (1995) estimated that 22 to 50% of the US dairy farms are contaminated with E. coli O157:H7. Higher estimates should be considered for STEC prevalence when taking into account other serotypes. The wide distribution of STEC on dairy farms was documented (Rahn et al., 1998) in the high prevalence rates reported for cows (58 of 274; 21.2%) and calves (68 of 135; 50.4%). In a recent study of 3 Japanese dairy farms (Ezawa et al., 2004), the prevalence rates of E. coli O157 were 33.7, 18.5, and 0% for heifers, cows, and calves, respectively. The high prevalence rate in heifers was attributed to their close contact during grazing. Other studies (Wells et al., 1991, 1992) illustrated the presence of a wide range of STEC serotypes in dairy cattle at different stages of production. Testing 1266 fecal samples from cows, heifers, and calves from 22 farms, a stockyard, and a packing plant (Wells et al., 1991) revealed the presence of E. coli O157:H7, O157:H–, and 27 other non- O157 serotypes (O10:H–, O15:H27, O22:H8, O22:H40, O25:H–, O26:H11, O45:H2, O45:H–, O76:H21, O84:H2, O84:H–, O103:H2, O103:H–, O111:H–, O116:H21, O121:H7, O145:H–, O153:H25, O163:H19, O171:H2, OX3 [the provisional designation for the O174 antigen]:H21, OX3:H–, OR [a rough O antigen]:H2, OR:H8, OR:H–, OUT:H–, and OUT:HUT [an untypeable H antigen]). Except for no detection of E. coli O157:H7, a similar distribution of non-O157 STEC was found when 1790 fecal samples from dairy cows and calves were tested (Wilson et al., 1992). The STEC strains included O2:HUT, O3:HUT, O4:H7, O4:H16, O4:H–, O6:HUT, O8:H8, O8:H16, O8:H–, O8:HUT, O9:H–, O11:HUT, O15:H–, O22:H1, O22:H8, O26:H–, O32:H7, O32:H16, O32:H–, O32:HUT, O40:HUT, O43:H2, O43:H6, O43:H12, O82:H–, O87:H–, O103:H2, O103:H6, O103:H12, O103:H16, O103:H39, O103:HUT, O106:HUT, O109:H16, O111:H–, O113:H–, O117:H–, O117:HUT, O119:H16, O121:H7, O121:HUT, O146:H–, O153:H7, O153:H32, O153:H–, O153:HUT, O163:HUT, OX3:H7, OX3:H16, OX3:H21, OX3:H39, OX3:H–, OX3:HUT, OX8 [a provisional designation for a new O antigen]:HUT, OUT:H2, OUT:H3, OUT:H6, OUT:H7, OUT:H8, OUT:H12, OUT:H16, OUT:H21, OUT:H40, OUT:H–, and OUT:HUT. Similar trends were also found in Japan (Tada et al., 1992; Furuhata et al., 1999), where members of the O26, O111, O145, and O157 serogroups (Tada et al., 1992) and 84 non-O157 STEC serotypes (Furuhata et al., 1999) were detected in dairy cattle feces. Furuhata et al. (1999) indicated that different serotypes were associated with specific geographical locations or climates and suggested that certain STEC serotypes may have resistance to hot or cold climates. With regard to sex effects on STEC shedding by dairy cattle, only one study was found (Montenegro et al., 1990). Various STEC serotypes (O3:H–, O10:H21, O22:H8, O39:H40, O75:H8, O82:H8, O82:H40, O91:H10, O104:H21, O105:H18, O113:H21, O116:H21, O126:H20, O126:H21, O136:H12, O139:H8, O156:H21, O157:H7, OR:H18, OUT:H16, and OUT:H29) were recovered from 17 and 9% of the 47 cows and 212 bulls tested, respectively. To better define dairy cattle as reservoirs of STEC, published reports on STEC prevalence in dairy cattle were evaluated.
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PREVALENCE OF STEC IN DAIRY CATTLE
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Prevalence rates of STEC in dairy cattle are summarized in Table 4. With 2 exceptions (Mechie et al., 1997; Bonardi et al., 1999), the prevalence rates of E. coli O157:H7 were based on one-time sampling of cattle feces. In these 2 studies, multiple samples (monthly for 15 mo or 1 yr, respectively) were tested. In Canada (Jackson et al., 1998), a very high prevalence rate (59 of 95; 62.1%) was found in a dairy farm that was associated with a child infection with E. coli O157:H7. In the US, E. coli O157:H7 prevalence rates ranged from 0.2 to 8.4% for cows, from 1.6 to 3.0% for heifers, and from 0.4 to 40.0% for calves. In Canada, Italy, Japan, and the UK, the corresponding ranges of E. coli O157:H7 prevalence rates were 0.3 to 16.1%, 10.0 to 14.1%, and 1.7 to 48.8%, respectively. These data emphasized the significant impact of animal age on epidemiology of E. coli O157:H7 as illustrated in the higher prevalence rates for younger (2- to 24-mo old) than for older cattle. Testing dairy cattle on 10 Dutch farms (Heuvelink et al., 1998) revealed prevalence rates of E. coli O157:H7 ranging from 0.8 to 22%, with calves (4- to 12-mo old) having the highest rate (21%). High prevalence rates were also reported for young beef cattle (Hancock et al., 1997c) and were attributed to the greater susceptibility to colonization for calves and heifers than for cows (Hancock et al., 1998). Prevalence rates of E. coli O157:H7 among dairy calves also appear to be affected by age. For example, the prevalence rate increased from 1.4% (6 of 423) before weaning to 4.8% (25 of 518) after weaning (Garber et al., 1995). Testing a large number of calves from 60 dairy herds in Washington State revealed that E. coli O157:H7 was more prevalent in weaned (7 of 1083; 0.65%) than in unweaned (0 of 649; 0%) calves (Hancock et al., 1994).
Factors that may affect the prevalence of E. coli O157:H7 in dairy cows were evaluated (Hancock et al.1994; Fitzgerald et al., 2003). In the study by Hancock et al. (1994), similar prevalence rates were reported for lactating (2 of 1273; 0.16%) and dry (1 of 477; 0.21%) cows. In contrast, a higher prevalence rate (43% vs. 22%) was reported for lactating cows than for dry cows (Fitzgerald et al., 2003). The time of fecal sampling was shown (Fitzgerald et al., 2003) to affect the number of dry cows shedding E. coli O157:H7 (28% for a.m. vs. 17% for p.m.) but not the lactating cows (average, 43%). Parity and DIM did not influence the number of cows shedding E. coli O157:H7 (Fitzgerald et al., 2003). The higher prevalence rates reported by Fitzgerald et al. (2003) could be attributed to the hot weather during the time of fecal sampling (August) in New Mexico. In the study by Hancock et al. (1994), however, the reported prevalence rates were average values of fecal testing of different dairy farms over a 1-yr investigation in Washington State.
Prevalence rates of E. coli O157:H7 in culled dairy cows have been variable. For example, prevalence rates ranging from 0.5% in Canada (Clarke et al., 1994) to 16.1% in the UK (Chapman et al., 1997) were reported. The 16.1% prevalence rate (Chapman et al., 1997) was much higher than the rates (1 to 2%) reported for younger dairy cows in the UK (Chapman et al., 1993) or in the US (Hancock et al., 1994). Prevalence rates for culled dairy cows ranged from 0.9 to 3% in New York State (USDA-APHIS-VS, 1996b). Based on data from 91 dairy farms, Garber et al. (1999) showed a higher prevalence rate (2.8% vs. 0.9%) for E. coli O157:H7 in culled cows than in those in production. Rice et al. (1997) tested fecal samples from culled dairy cows on the farm (205 cows from 19 herds) and at slaughter (103 cows from 15 herds) in Idaho, Oregon, and Washington State and reported that 3.4 and 3.9% of the cows on the farm and at slaughter, respectively, were positive for E. coli O157:H7. Dairy cattle with downer cow syndrome are those suffering from assorted maladies (e.g., mastitis, calving paralysis, and milk fever) and/or injuries (e.g., during transport) that render them immobile to various degrees (Correa et al., 1993). If their condition does not improve, they are culled from the production herd (Faith et al., 1996; Troutt and Osburn, 1997) and enter the food chain as ground beef. As a result, downer dairy cows harboring STEC at slaughter can be a health risk to humans. This potential risk was recently evaluated at 2 packing plants in Wisconsin over a 6-mo (May to October) period (Byrne et al., 2003). The prevalence rate was higher for downer (10 of 203; 4.9%) than for healthy (3 of 201; 1.5%) cows that were harvested at the same time and were from similar geographical locations.
Prevalence rates of non-O157 STEC in dairy cattle are also summarized in Table 4. Multiple sampling (monthly over a 1-yr period) of cattle feces was used in 2 studies (Hancock et al., 1997a; Conedera et al., 2001) but one-time sampling was used in the others. Worldwide, the prevalence rates ranged from 0.4 to 52.0% for cows, from 1.7 to 74.0% for heifers, and from 1.3 to 68.7% for calves. Non-O157 STEC were more prevalent in dairy cattle than E. coli O157 (Table 4). In addition to detecting strains that belonged to 39 O serogroups, a total of 77 STEC serotypes were isolated from dairy cattle feces (Table 4). Of these, 15 (O2:H29, O22:H8, O26:H11, O103:H2, O103:H–, O105:H18, O111:H8, O111:H–, O113:H21, O145:H–, O153:H25, O163:H19, OX3:H21, OUT:H2, and OUT:H25) are known to cause HUS and 20 (O7:H4, O15:H27, O22:H40, O22:H–, O25:H–, O45:H2, O45:H–, O70:H11, O84:H2, O91:H–, O113:H2, O113:H4, O119:H–, O125:H–, O146:H21, O171:H2, OR:H–, OUT:H18, OUT:H21, and OUT:H–) are known to cause other illnesses (WHO, 1998).
In contrast to the E. coli O157:H7 data, there was no clear age effect on the prevalence of non-O157 STEC (Table 4). Interestingly, Nielsen et al. (2002) reported variations in prevalence of non-O157 STEC within Danish dairy calves. A higher prevalence rate (8.6% vs. 0.7%) was found for older (2 to 6 mo) than for younger (<2 mo) calves. Rugbjerg et al. (2003) also reported a higher prevalence rate (11.8% vs. 2.1%) in older (3 to 4 mo) than in younger (1 to 2 mo) calves.
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PREVALENCE OF STEC IN RAW MILK
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Prevalence of STEC in raw milk was determined in a limited number of studies focusing on E. coli O157:H7 in bulk tanks (Wells et al., 1991; Murinda et al., 2002). In the US, a low prevalence rate (2 of 268; 0.75%) was reported in Tennessee (Murinda et al., 2002) and a relatively higher rate (1 of 23; 4.3%) was reported in Wisconsin and Washington State (Wells et al., 1991). Similar (2 of 35; 5.7%) and higher (6 of 37; 16.2%) prevalence rates were reported in the UK (Mechie et al., 1997) and Canada (Cardinal, 1993), respectively. A 2-yr study of bulk milk in the UK (McKee et al., 2003) revealed a lower prevalence rate for STEC, in general, than those reported for E. coli O157:H7 (Wells et al., 1991; Cardinal, 1993; Mechie et al., 1997). The presumed route of STEC transmission to raw milk is fecal contamination during milking. This could be eliminated by improving sanitation during the milking process, as shown in a Taiwanese study (Chiueh et al., 2002). Raw milk samples from 407 cows tested negative for STEC, although 8 cows in the production herd tested positive (Chiueh et al., 2002).
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DAIRY CATTLE AS TRANSIENT CARRIERS OF STEC
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Prevalence rates of STEC in cattle have significant fluctuations over time (Hancock et al., 1998). Repeated fecal testing of cattle herds demonstrated that STEC are, at least occasionally, present on most farms (Hancock et al., 1997a, b). In general, cattle have not been reported as long-term carriers of STEC, and fecal shedding has not been associated with any cattle disease (Garber et al., 1995; Hancock et al., 1997b,c). Studies with dairy cattle showed the transient presence of E. coli O157:H7 (Hancock et al., 1994; 1997a). In an initial study (Hancock et al., 1994), E. coli O157:H7 was found on 5 of the 60 dairy farms that were sampled once. In a following study (Hancock et al., 1997a), 8 of the initially negative farms were sampled monthly for 3 to 12 mo, and E. coli O157:H7 was detected in 4 of those farms. It was concluded, therefore, that repeated sampling is needed to establish an accurate prevalence status of STEC.
Fecal shedding of STEC by dairy cattle has been shown to follow a seasonal trend. In the US, the highest prevalence rates of E. coli O157:H7 in dairy cattle were in warm weather (Hancock et al., 1997a, b; Garber et al., 1999), which is consistent with the timing of most human illness outbreaks (USDA-APHIS-VS, 1997). Monthly fecal sampling of dairy cattle in Idaho, Oregon, and Washington State (Hancock et al., 1997b) over a 6-mo period (July to December) revealed a sharp decline in E. coli O157:H7 prevalence in cold weather (November and December). An investigation of E. coli O157 on 9 dairy herds for 13 mo revealed prevalence rates that were several times higher in warm (June to October) than in cold (December to March) weather (Hancock et al., 1997a). The prevalence of E. coli O157:H7 peaked at 2.6% in June and was lowest (0%) in December. In another study covering 20 states (CA, FL, ID, IL, IN, IA, KY, MI, MN, MO, NM, NY, OH, OR, PA, TN, TX, VT, WA, and WI), Garber et al. (1999) tested 4361 fecal samples from cows on 91 dairy farms over a 6-mo period (February to July) and reported a higher prevalence rate (52.9% vs. 7.0%) in the summer than in the spring. Herds in the Southern states had a higher prevalence rate (61.9% vs. 12.9%) than those in the Northern states. Hancock et al. (1997b) observed a significant correlation between multiple fecal testing of dairy herds and prevalence of E. coli O157:H7 and reported that some herds had tendencies to have higher or lower prevalence rates that were somewhat stable over time.
In a 1-yr study, similar seasonal effects on E. coli O157:H7 prevalence in dairy cows, heifers, and calves were detected in Canada, Denmark, Italy, and the UK. In the UK (Mechie et al., 1997), testing of 3593 fecal samples showed the highest prevalence rates (average, 8.3%) to occur from May to July and the lowest rate (0%) to occur from December to April. In Denmark (Rugbjerg et al., 2003), testing of 1706 fecal samples also showed a higher prevalence rate in summer than in winter (9.9% vs. 2.9%). In Northern Italy (Bonardi et al., 1999), testing of 450 fecal samples revealed a higher prevalence rate (17.5% vs. 2.9%) in the warm months (April to October) than in the cold months (November to January). In the same region (Conedera et al., 2001), testing of 650 fecal samples showed higher prevalence rates in August and September (average, 20%) than in January and February (average, 15%). In Canada (Van Donkersgoed et al., 1999), testing of 1247 fecal samples from culled cows at slaughter also showed E. coli O157:H7 to be most prevalent from June to August. Except for one investigation (Thran et al., 2001), no studies evaluating prevalence of non-O157 STEC over time were found. Testing fecal samples from 23 heifers over 1 yr resulted in detecting STEC only during winter at a prevalence rate of 9.5% (Thran et al., 2001). Interestingly, the STEC isolates belonged to 2 non-O157 serotypes (O26:H– and OUT:HUT).
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PATHOGENICITY OF STEC FROM DAIRY CATTLE
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A few studies evaluated distribution of the virulence genes among STEC isolates from dairy cattle (Sandhu et al., 1996; Wilson et al., 1996; Byrne et al., 2003). For example, Wilson et al. (1996) reported the presence of the eae gene in 37% of O157:H7 and non-O157:H7 STEC isolates. Sandhu et al. (1996) also showed that the eae gene was more frequently found (42% vs. 18%) in STEC from calves than from cows. In the same study, 35% of E. coli O157:H7 strains were positive for the eae gene. Of the eae-positive isolates, 73% produced only Stx1, suggesting a strong association between certain O sero-groups (O5, O26, O69, O84, O103, O111, O145, and O157) and the eae gene. It was concluded, therefore, that Stx1 production is more frequently associated with eae-positive than with eae-negative STEC strains (Sandhu et al., 1996). In another study, 57 E. coli O157:H7 isolates were tested for the presence of the stx1, stx2, eae, and ehxA genes (Byrne et al., 2003). Results showed 67% of the isolates to have the 4 genes, whereas the remaining isolates had various combinations of 3 genes at different rates (19% had stx1, eae, and ehxA; 9% had stx2, eae, and ehxA; and 5% had stx1, stx2, and eae). The presence of these virulence factors was evaluated for O157 (Table 5) and non-O157 STEC (Table 6) isolates from dairy cattle.
With regard to E. coli O157 (Table 5), some isolates had stx1, stx2, or both genes. The ability of this serotype, as well as other non-O157:H7 STEC strains, to cause human illnesses depends on the production of Stx1, Stx2, or both toxins (Karmali et al., 1985). All E. coli O157:H7 isolates that were tested for the presence of the eae gene gave positive results (Table 5). Except for one isolate (Byrne et al., 2003), all of the tested ones also were positive for the ehxA gene. Beutin et al. (1994) investigated human infections with O157 and non-O157 STEC (O26:H11, O111:H8, and O145:H–) and reported that they had the eae and ehxA genes at high rates (92 and 88%, respectively). Beutin et al. (1994) also reported that E. coli O157:H7 was responsible for the most severe illnesses (hemorrhagic colitis and HUS). The data in Table 5, therefore, suggest a high level of pathogenicity for several E. coli O157:H7 isolates of dairy cattle origin (Murinda et al., 2002; Byrne et al., 2003).
Table 6 shows that 44 STEC serotypes and members of 2 O serogroups (O87 and O88) had only stx1, whereas 69 serotypes and members of 11 O serogroups (O1, O8, O15, O21, O28, O104, O111, O158, O172, O174, and O175) had only stx2. Additionally, 41 serotypes and members of 6 O serogroups (O23, O38, O55, O73, O123, and O125) had both genes. Although isolates from 4 serotypes had only stx1 (OUT:H– and OUT:HUT) or stx2 (OUT:H8 and OUT:H21), the isolates from each of the remaining serotypes exhibited different toxin genotypes. For example, isolates from each of the O22:H–, O98:H–, O113:H21, O145:H21, O153:H25, O153:H–, and OUT:H7 serotypes had stx1 or stx2. Isolates from each of the O105:H18 and O111:H–serotypes had stx1 or both stx1 and stx2, whereas those from each of the O22:H16, O45:H8, O45:H9, O45:HUT, O82:H8, O116:H21, O153:H19, O153:HUT, O157:H–, OUT:H16, OUT:H18, OUT:H21, OUT:H–, and OUT:HUT sero-types had stx2 or both stx1 and stx2. Finally, isolates from each of the serotypes O45:H–and O126:H– had stx1, stx2, or both genes. Table 6 shows that 20 STEC serotypes (in bold) commonly isolated from dairy cattle are known to cause HUS (WHO, 1998; Blanco et al., 2003). Several other serotypes (O1:H7, O7:H4, O15:H27, O22:H16, O22:H–, O45:H2, O45:H–, O70:H11, O80:H–, O82:H8, O84:H2, O104:H21, O116:H21, O126:H21, O126:H–, O132:H–, O145:H16, O146:H21, O153:H2, O171:H2, OR:H–, OUT:H18, OUT:H19, and OUT:H21) in Table 6 are also known to cause diarrhea, bloody diarrhea, or hemorrhagic colitis (WHO, 1998).
Based on potential toxicity by having stx1 and/or stx2 genes, it is clear from Table 6 that it is not necessary for an isolate to have and express both genes to cause human illnesses. With regard to other virulence genes (eae and ehxA), unfortunately, the 20 STEC serotypes in Table 6 that are known to cause HUS were not evaluated for presence of the ehxA gene. Of these serotypes, 5 (O5:H–, O26:H–, O103:H2, OUT:H2, and OUT:H–) were evaluated for presence of the eae gene, and only 2 (O5:H–and O103:H2) tested positive. The ability of these eae-positive isolates to produce a functional intimin, however, was not reported. Investigating STEC pathogenicity (HUS cases) as affected by the presence of eae and ehxA genes (Karch et al., 1997) revealed that most STEC isolates were eae-positive. Several STEC strains involved in severe human illnesses (e.g., HUS), however, have lacked this gene or did not express a functional intimin (Keskimäki et al., 1997). This suggests that STEC strains lacking the eae gene can colonize the small intestine by expressing additional adherence factors. Studies of STEC in HUS patients showed that both eae and ehxA genes were found in virtually all E. coli O157 strains (Beutin et al., 1994) but were more variably present among the non-O157 strains (Neill, 1997). The data in Tables 5 and 6 support this conclusion. Although the eae and ehxA genes appear to be more common in the STEC strains associated with human illnesses, they are not absolutely required for pathogenicity, as strains lacking these genes have been shown to cause human illnesses (Neill, 1997).
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CONCLUSIONS
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The role of dairy cattle and their products in human infections with STEC was evaluated. These pathogens cause human illnesses ranging from mild diarrhea to the life-threatening HUS. Most STEC outbreaks were traced to the consumption of ground beef or dairy products. Contact with dairy farm environments by urban visitors also caused outbreaks of human illnesses. Long-term and short-term testing of dairy cattle feces worldwide showed high prevalence rates for O157 (ranging from 0.2 to 48.8%) and non-O157 STEC (ranging from 0.4 to 74.0%). Shiga toxin-producing E. coli were also isolated from raw milk, milk filters, and dairy products such as yogurt and soft cheeses. Dairy cattle, therefore, are considered reservoirs of STEC. The data summarized in this review showed 193 STEC serotypes to derive from dairy cattle origin. Of these serotypes, 24 have been isolated from HUS patients. Considering the wide distribution of STEC on dairy farms, the high prevalence rates reported, and the isolation of several sero-types of high virulence from dairy cattle or their products, long-term strategies to assure safety of foods from dairy cattle should be developed. These strategies should focus on establishing educational programs to bring awareness of the STEC problem to dairy farmers, processors, and consumers. Developing and implementing pre- and postharvest control methods to effectively decrease STEC carriage by dairy cattle and to eliminate contamination of their products during processing are essential steps toward sustaining a competitive dairy industry.
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ACKNOWLEDGEMENTS
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The authors acknowledge the support of the USDA Integrated Research, Education, and Extension Competitive Grants Program (Grant No. 2001-05062).
Received for publication March 31, 2004.
Accepted for publication August 31, 2004.
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ABSTRACT
INTRODUCTION
