Verocytoxigenic<i>Escherichia coli</i>in animal faeces, manures and slurries

Summary, 94S Introduction, 94S Outbreaks, 95S Prevalence, 96S Survival and transmission, 98S Control measures, 99S Treatment of manure/slurries, 99S Production of organic produce, 100S Farm visits by children/contact with pets, 100S Conclusions, 100S References, 100S Animal wastes and effluents from farming operations, including manures and slurries, are frequently applied as fertilizer to land used for crop or silage production and cattle grazing. It is well documented that potentially harmful pathogens including verocytoxigenic Escherichia coli (VTEC) are shed in animal faeces and there is growing concern in many countries about the number of sporadic and outbreak cases of VTEC attributable to direct contact with faecal material either as a result of handling contaminated mud in fields or ingestion of produce grown in contaminated manures or slurries. VTEC has been detected in the faeces of ruminant and non-ruminant farmed animals, wild animals, domestic pets and birds and the pathogen appears to be well adapted to survive in animal faeces and can persist for extended periods ranging from several weeks to many months. Because of this persistence these materials are important as potential vehicles for transmission within herds, farms, the fresh food chain and the wider environment. Appropriate handling of bovine faeces is necessary to control spread of this pathogen and to limit the significant risks of human infection. It may be necessary to hold manure/slurry for extended periods prior to spreading on farmland, or for use in the production of food crops, particularly foods that are to be consumed in the raw or minimally processed state. Alternatively, it may be necessary to apply processes such as composting, heat drying or digestion which can expedite the decline of pathogens including VTEC in manures. However, there is a need for research work to develop economical and practical systems for treatment of manures and slurries. The risk from direct contact with faecal material at farms and petting zoos is also recognized and many public health authorities have put forward measures for strict practices to limit the risk of infection, particularly for young children visiting these environments. Animal wastes are a valuable source of nutrients including N, P2O5 and K2O and are used extensively in farming practices. Animal wastes and effluents from farming operations include faeces, manures and slurries. Faeces are generally regarded as freshly deposited faeces, manures are faeces which may have undergone some period of storage and slurries are mixtures which include manure, urine and left over feed that is held in a tank or pit generally under anaerobic conditions. These effluents are frequently applied as fertilizer to land used for crop or silage production and cattle grazing. It is well documented that potentially harmful pathogens are shed in animal faeces and may remain viable for considerable periods of time (Bolton et al. 1999) posing a risk of transmission of pathogens both by direct contact from handling contaminated mud in fields or ingestion of produce grown in manures or slurries which contain harmful pathogens. Emerging pathogens such as verocytoxigenic Escherichia coli (VTEC) pose a considerable risk in this regard because of their infectious dose which is reportedly as low as 50 organisms (Tilden et al. 1996). To date, E. coli O157 has been considered the most important VTEC strain in terms of severity of human illness. The pathogen results in serious illness in about a third of all cases and chronic complications in a smaller number of cases (ca.10%). The vulnerable sectors of the community (children and the elderly) are at most risk of developing severe VTEC infection, making it a very emotive issue in public health and across the food and agricultural industries. Apart from serotype O157:H7 four other serogroups (O111, O26, O103 and O145) have now been identified by the World Health Organization (WHO) as emergent pathogens in Europe. It is not only the survival of vegetative VTEC cells in the environment that is of concern. The genes coding for verotoxins in E. coli O157:H7 are carried by lysogenic phages, which are mobile genetic elements. These vt genes may move through the animal population or environment within vegetative (VTEC) cells, or by the transduction of VT-encoding phages among existing E. coli populations. Little is known about the importance of phages as reservoirs of such genes or the significance of their spread among different enterobacterial strains. A recent study has shown that verotoxigenic phages capable of infecting E. coli O157:H7 can survive in sewage and in water, suggesting that they may represent a potential source of pathogenicity factors. Significantly, they survived longer than bacterial cells in water exposed to adverse environmental conditions and they were more resistant to chlorination of sewage (Muniesa and Jofre 1998; Muniesa et al. 1999). If the VT phages have a broad host specificity, i.e. they are able to infect a wide range of E. coli serogroups and/or serotypes, they may constitute a very important reservoir of VT phages for human pathogenic strains. More research on the mobility and host specificity of VT phages is needed before these questions can be answered. There is a considerable literature on VTEC, in particular E. coli O157:H7 in animal wastes. This paper outlines the importance of animal wastes as a vector for VTEC and reviews the prevalence and persistence of the pathogen in animal faeces, manures and slurries and outlines clinical cases, which have been linked to VTEC in animal wastes. Measures, which may prove useful in the control of VTEC in these matrices, are presented and discussed. The reputation of E. coli O157:H7 as the ‘hamburger bug’ has long been called into question as many other foodstuffs including unpasteurized apple cider (CDC 1997), vegetables (Michino et al. 1998), dairy products (Reid 2000) and water (Anon. 2000) have now been identified as vehicles of infection. Person-to-person spread is also recognized as an important mode of transmission of the pathogen, particularly among vulnerable groups such as young children and the elderly, and in settings such as creches and nursing homes (Al-Jader et al. 1999). However, while food, water and person to person spread still account for a significant proportion of outbreaks, there is growing concern in many countries about the number of sporadic and outbreak cases attributable to direct contact with faecal material. Table 1, modified from Tozzi et al. (2001), lists a number of outbreaks of E. coli O157:H7 linked to direct contact with faecal material. Some of these cases involved direct contact with animals or faecally contaminated mud while others result from handling of fruit/vegetables contaminated with faecal material or manure. It is interesting to note that four of these nine outbreaks were reported in the last 3 years showing the growing importance or awareness/reporting of this route of transmission. In England and Wales, between 1995 and 1998, there were 85 outbreaks of E. coli O157:H7 of which 12 (14%) were associated with visits of the infected person to open/commercial farms or outdoor activities on farmland including camping and music festivals (Smith et al. 2001). The mode of transmission in these cases was linked to direct or indirect contact with animal faeces. Epidemiological evidence also suggests that this mode of transmission is responsible for a significant portion of sporadic cases of E. coli O157:H7 infection in the UK (Adak et al. 2000). This was also demonstrated by a prospective, case–control study of sporadic cases undertaken in Scotland (Locking 2000). In this survey, 183 case studies were covered and the results indicated that contact (or likely contact) with animal faeces could account for almost 50% of these cases. A higher risk of infection was associated with contact with cattle and work-related exposure on farms. This study confirmed the evidence from other studies that direct contact with faecal material is a major transmission route for E. coli O157:H7. Sporadic cases have been reported in other countries including the Netherlands where a case of E. coli O157:H7 resulted in haemolytic uretic syndrome in a young child (1.5 years) was associated with a visit to a petting zoo (Heuvelink et al. 2000). The epidemiological evidence suggested that faecal droppings from goats and sheep at the zoo were the source of the pathogen. The data in Table 1 indicate that there is a strong seasonal link with peaks of E. coli O157:H7 infection occurring in summer or early autumn and secondly a geographical bias with most outbreaks being reported in the UK. The seasonal effect is no doubt partly influenced by increased shedding of E. coli O157:H7 in ruminant animals during spring/late summer and has been well documented in the literature (Blanco et al. 2001). It may also be a reflection of increased outdoor activity by people in the summer/early autumn and thus increased exposure of individuals to the risk of infection. The geographical bias is reflective of a high prevalence of E. coli O157:H7 in these countries with the UK having the highest reported incidence of E. coli O157 infections in Europe and the USA/Canada also report high numbers of infection in relation to the rest of the world. No outbreaks to date of non-O157 VTEC have been linked to outdoor activities or direct contact with faecal material, although this is possibly related to poor detection and surveillance systems for these pathogens. Cattle and their faeces have, for a number of years, been considered the primary source of VTEC and the reported incidence of E. coli O157:H7 in cattle faeces varies widely depending on the geographical location and the season. The results of studies on the prevalence of VTEC O157:H7 in cattle are shown in Table 2 (modified from Blanco et al. 2001). The prevalence rates varied from 0.1% in studies carried out in Spain (Blanco et al. 1996, 1997) and Norway (Johnsen et al. 2001) to 62% in a Canadian Study (Jackson et al. 1998). As noted by Jordan et al. (1999), the concentration of VTEC in the faeces of naturally infected cattle has been poorly described in the literature. However, recent estimates suggest that the pathogen may be present in faeces from calves and heifers at levels ranging from 102 to 105 CFU g−1 (Himathongkham et al. 1999). There is a clear seasonal influence on VTEC with a peak incidence of faecal shedding of E. coli O157:H7 in spring and summer (Blanco et al. 2001). Studies on the serotypes of VTEC (O157 and non-O157 serotypes) present in cattle faeces are shown in Table 3 (modified from Blanco et al. 2001). The percentage of VTEC serotypes in cattle faeces ranged from 6% in a US study (Cray et al. 1996) to 71% in a French study (Pradel et al. 2000). Absence of routine cultural detection methods for non-O157:H7 mean that many countries do not have data on the prevalence of non-O157:H7 and it is certain that there is considerable underreporting on these pathogens. While cattle faeces remain an important vector of VTEC in the environment, it is now recognized that the strain characteristics of many bovine strains do not match the profile of human clinical isolates. Recent evidence has suggested that sheep are more important in terms of transmission to humans than was previously recognized. Indeed, several recent outbreaks of E. coli O157:H7 in the UK were epidemiologically linked to direct contact with sheep faeces. One such outbreak involved a group of boy scouts camping on a field which had previously been occupied by a flock of sheep. The faeces in the field and the sheep all screened positive for E. coli O157:H7 and the strain was identical to that isolated from the infected children (Strachan et al. 2001). Studies on the prevalence of E. coli O157:H7 in sheep faeces indicated that the pathogen is present at levels ranging from 0% (0/364) in a Norwegian study (Johnsen et al. 2001) to 4% (4/101) in a Dutch study (Heuvelink et al. 1998). A UK study reported a prevalence of 2% (22/1000) (Chapman et al. 1997). As noted in cattle, changes in diet, and other factors significantly modulate the rate of VTEC shedding. Some workers report significant seasonal differences in rates of shedding of VTEC by sheep (Kudva et al. 1996). VTEC have also been detected in the faeces of a wide range of non-ruminant animals, including domesticated, feral and wild species. In pigs, VTEC can cause oedema disease and may also be involved in postweaning diarrhoea syndromes. In general it is VTEC serotypes O138, O139 and O141 that are implicated in illness in pigs and these have not been linked to human illness. European studies determining the prevalence of human pathogenic VTEC strains in pigs in general have reported a very low prevalence. A Dutch study found only one of 145 pig faecal samples to be positive for E. coli O157:H7 (Heuvelink et al. 1999) while studies in Norway have reported the sporadic isolation of the pathogen (Johnsen et al. 2001). In contrast, a study in Chile reported that 69% of pigs were positive for E. coli O157, O111 and O26 (Rios 1999). While VTEC was not detected in poultry faecal samples in studies carried out in the Netherlands (Heuvelink et al. 1999) or the UK (Chapman et al. 1997), a number of studies have shown the presence of VTEC in wild bird droppings including gulls in the UK (Wallace et al. 1997) and pigeons in Rome (Dell'Omo et al. 1998). Escherichia coli O157 was detected in 0·9–2·9% of gull samples tested, indicating that these birds may play an important role in the spread of VTEC in the environment. While VTEC were isolated in the Roman study in pigeon droppings, none were human pathogenic serotypes and the role that pigeon droppings may play in the transmission of VTEC human infection is unclear. However, in the light of the presence of pigeons in many squares in large cities where people congregate to sit and to eat and drink, the public health issue in relation to pigeons requires further study. The faeces of domestic pets (dogs and cats) have also tested positive for VTEC including serotype O157:H7 (Trevena et al. 1996). Taking into account the close contact with family pets especially by children, their frequent presence in kitchens where food is prepared and consumed, they must be recognized as a substantial risk. Good hygiene and hand washing practices are therefore essential in any household where pets are present. It is evident that VTEC is widespread in animal faeces and therefore application of untreated manures to vegetables may pose a risk for transmission of VTEC to food. Infection can potentially occur through the direct hand to mouth route from handling of contaminated produce during harvesting or through consumption of contaminated products. Because of difficulties associated with detection, the presence of injured/stressed cells and those potentially in a viable but non-culturable state means that the prevalence figures reported on the levels of VTEC in faeces and manures represent a considerable underestimation of the actual figures. Considerable attention has been paid to the persistence of VTEC in cattle faeces, manures and slurries. The survival times for E. coli O157:H7 under different storage conditions are shown in Table 4. In experiments on the survival of E. coli O157:H7 in faeces outdoors on grass under ambient weather conditions in Ireland, this organism was capable of long-term survival (99 days) in faeces and in the underlying soil. The pathogen could be recovered directly from faeces on the grass for 50 days. When faeces were no longer visible on the grass, using enrichment techniques, the organism was shown to persist in the underlying soil for a further 49 days (Bolton et al. 1999). A similar study in the UK (Maule 2000) reported the survival of E. coli O157 in cattle faeces for >50 days but reported much shorter survival times in cattle slurry in which it fell to undetectable levels within 10 days. A study carried out in Ireland by McGee et al. (2001) investigated the survival characteristics of E. coli O157:H7 in bovine slurry from cattle fed two different diets: (i) silage and (ii) silage + concentrates. Slurry samples collected from freshly-agitated tanks were inoculated at a level of log10 6·0 CFU g−1 and stored in the laboratory at 10°C. Over a 12-week storage period, a 3·5 and 5·5 log reduction was observed in slurry from cattle fed a silage and silage plus concentrate diet, Escherichia coli O157:H7 was in the slurry for to 3 indicating the potential for transmission of the organism into the environment. There have been studies on the persistence of coli O157:H7 serotypes in animal faeces. However, one study which investigated the survival of E. coli O26, and O157 in bovine faeces et al. 1999) stored at and demonstrated that all pathogens survived for to weeks at persistence has been reported in sheep with survival for days at or reported by et al. However, et al. a study on the survival of E. coli O157:H7 in poultry and slurries and reported that the pathogen had a reduction time ranging from a at to weeks at The of E. coli O157:H7 in poultry and as to bovine and and reflective of the higher levels of in poultry manure. It is also important to note the of VTEC to survive for extended periods of weeks in the faeces of such as and pigeons et al. 2000). the previously in relation to persistence of VTEC in the much of food animal faeces, apply to VTEC persistence in the faeces of potentially more mobile and other animals into contact with farmed The long-term survival of E. coli O157:H7 in the need for to environmental spread of this the persistence of VTEC in and slurries it is clear that the application of untreated animal products to food produce considerable risks to food Apart from potential infection from handling of this produce transmission a recent study et al. demonstrated the transmission of E. coli O157:H7 from contaminated and water to and of viable pathogens from the of indicating that E. coli O157:H7 to in and was thus from the of by of This an risk in consumed in a raw or minimally prepared state. Because of the persistence of VTEC in faeces, and slurries, these materials are important potential vehicles for transmission. Appropriate handling of bovine faeces is necessary to control spread of this pathogen and in the significant risks of human infection. This from direct contact with or slurry within farming farming or during contact with contaminated of such risks may on to contact between and fresh There are in the literature of processes which can expedite the decline of pathogens including E. coli O157:H7 in manures. treatment processes used include composting, heat drying and A study carried out by and investigated the effect of drying and/or with on the of E. coli O157:H7 in fresh manure. reported a log of E. coli O157:H7 over days in the manure, at This decline in numbers was by an in and of in the manure. Over the period of time the decline in numbers of the pathogen was increased log by drying the to a of by exposure to to a level of of the is a for of animal only a of is and the may not be under strict conditions of and of the material, of can be which be to pathogens including E. coli O157:H7. carried out by et al. (2001) has shown that E. coli O157:H7 inoculated at a level of log10 CFU g−1 was in manure. This that composting, carried out can a for pathogen particularly to slurries include anaerobic digestion at with 12 days for pig slurry or days for cattle and poultry The of or to the to 12 for at 2 also result in significant pathogen reduction et al. 2001). to the prevalence of VTEC in could of animals et al. with a to and in such major to of the of VTEC through animals, feed and environments. Some results on the potential role for of E. coli O157:H7 using have been reported by et al. present there is no evidence to the that organic produce is more or than farmed However, it is recognized that there is a potential risk to food from the use of animal wastes in in terms of pathogen transmission and is been in the and the Production of organic products in the is by In the a organic that is with developing for foods These for organic farming of the risk of of pathogens from manure. in the are from using raw on within days of or are to use which has been to pathogens. must also of they are using on the soil and it was As a result of some outbreaks where young children infected as a result of handling animal at petting many public health authorities have the and to be visiting petting zoos and farms where young children are more likely to in direct contact with animals, E. coli O157 UK is needed about the role of farms in and farms can be in risks for be with hand washing and the public need to be about the risks and and before and during such to certain practices such as washing petting the animals and hand to mouth contact visiting farms some of the is a in the risk to in direct contact with VTEC is frequently present in animal wastes and can persist in these for considerable periods of time posing a risk of transmission to humans direct contact from handling animals or faecal material or handling or consumption of contaminated There is a need to develop practical and economical to pathogens from animal are also needed on the potential for of pathogens on manure, especially for use in and These data be into risk and used to develop for storage and treatment and land application of animal wastes. in direct contact with faecal material or where in contact with animal wastes the associated risk and hygiene practices.

Récupéré en direct depuis OpenAlex et désinversé. Les résumés ne sont pas conservés dans cette base de données : les index inversés représentent 8,6 Go des 9,3 Go de texte de la base, et le serveur dispose de 13 Go libres.