Cattle and sheep farms as reservoirs ofCampylobacter

Summary, 104S Introduction, 104S General aspects of Campylobacter, 104S Historical aspects, 104S Biology of thermophilic campylobacters, 105S Cycles of growth and survival, 105S The role of ruminant animals in human infection, 105S General epidemiology in humans, 105S The significance of ruminant sources of infection, 105S The seasonality in human infection, 106S The incidence of Campylobacter in cattle and sheep, 107S Isolation rates at slaughter, 107S Patterns of Campylobacter shedding on the farm, 108S Seasonal variation in dairy herds, 108S Factors affecting shedding in dairy herds, 108S Campylobacter shedding by sheep, 109S Young animals on the farm, 109S Effects of lambing on colonization, 109S Colonization and shedding by calves, 109S Contamination of the farm environment, 109S Potential sources of new infection in adult cattle, 110S Conclusions, 110S References, 111S Aim: This is a review of the natural Campylobacter colonization and transmission among ruminant livestock in the dairy farm environment. Methods and Results: Using cultural detection methods and enumeration techniques the distribution of Campylobacter in ruminant animals at birth, on the farm, at slaughter and in the farm environment have been examined. Colonization and shedding rates are higher among young animals while patterns of shedding in adult animals may be seasonal. Stored and land‐dispersed slurries provide a reservoir for scavenging birds and flies and a source for runoff. Conclusions: The dairy farm plays a significant role in the dissemination of Campylobacter sub‐types that can cause disease in the human community. Significance and Impact of Study: An understanding of the role of the dairy farm in the environmental cycle of Campylobacter is required in order to devise intervention strategies. Campylobacter jejuni is the most commonly isolated bacterial pathogen associated with diarrhoea in the UK (Ketley 1997) and other industrialized countries (Mead et al. 1999). Historically, the North‐west region of England has had a higher than average rate of infection (Jones and Telford 1991) but otherwise the data in that area reflect the trends observed in the UK national data, i.e. an increase over the years in the annual number of cases since 1981, and a late spring/early summer annual peak. There is also a lower secondary autumn peak. Campylobacter jejuni colonizes the gastrointestinal tract of a broad range of animals but the most important risk factor for human Campylobacter infection is widely held to be the handling and consumption of raw poultry and cross‐contamination to uncooked products (Tauxe 1992). However, there is now a growing body of molecular evidence that suggests the significance of non‐poultry sources of human clinical infection has been underestimated. This review focuses on the significance of Campylobacter colonization of cattle and sheep, the incidence and rate of shedding among these animals and the role of the dairy farm as a reservoir of Campylobacter infection. For most of the last century Campylobacter was recognized exclusively as an animal pathogen but the description of a suitable selective isolation medium and exacting growth requirements (Skirrow 1977) was required before the role of Campylobacter, as an aetiological agent of human enteritis, was fully recognized. During the last 25 years new pathogenic species have been assigned to the genus. Although a number of these have been implicated in human enteritis the most common by far are the so‐called ‘thermophilic’ campylobacters of which, C. jejuni causes more than 90% of Campylobacter enteritis in the UK. The other ‘thermophilic species’ strictly include C. coli and C. lari but C. hyointestinalis is also associated with enteric disease and can be isolated from cattle. Thermophilic campylobacters are small, non‐spore forming, Gram‐negative bacteria which are vigorously motile by means of a single polar flagellum at one or both ends of the cell. Unique properties of the flagellum impart increased cell motility in highly viscous environments (Alm et al. 1993) and allow the organism to colonize mucus within the intestinal and caecal crypts (Lee et al. 1986). The flagellum is the most intensively studied virulence determinant. Thermophilic Campylobacter neither ferment nor oxidize carbohydrate but obtain energy from oxidation of amino acids or tricarboxylic acids. They have simple nutritional requirements and can be grown on a peptone base (Grau 1991) but they compete poorly with other flora. They grow best in an atmosphere containing 5–10% oxygen and are described as microaerophilic to distinguish their preferential use of oxygen as a terminal electron acceptor under reduced oxygen tensions (Krieg and Hoffman 1986). The ‘thermophilic’ species are so‐named not so much for their ability to grow at high temperatures but to emphasis their inability to grow below 30°C. Such temperature growth constraints, when considered along with their microaerophilic nature, suggest that they are unlikely to find suitable conditions for growth outside of the mammalian gut. We must also assume that thermophilic Campylobacter cannot amplify on food or in water and therefore they should be considered ‘food‐borne’ rather than ‘food‐poisoning’ organisms. Indeed, they do not survive well at ambient temperatures. Further, thermophilic campylobacters are reportedly sensitive to many environmental factors, such as high temperatures, atmospheric concentrations of oxygen, oxygen species, such as free radicals and peroxides, and to desiccation (Griffiths and Park 1990). This leads to the inevitable question – how does such a ‘fragile’ organism cause disease so frequently? The fact that Campylobacter outbreaks are rare, accounting for only 2% of outbreaks in England and Wales where an aetiological agent was identified between 1994 and 1999 (Frost et al. 2002) is consistent with the assumption that Campylobacter do not grow on food. However, recent biochemical investigation (Kelly 2001) and the recently published genome seqence data (Parkhill et al. 2000) support the notion that C. jejuni is a versatile and metabolically active organism which may be able to exploit more diverse environments than the described constraints suggest. The major environmental reservoirs of thermophilic campylobacters are the intestines of warm‐blooded mammals and birds, where it is thought that they are non‐pathogenic, at least in older animals (Griffiths and Park 1990). The intestines of host animals are therefore a critical site of amplification in the Campylobacter life cycle as this is where the maximum population size will occur. Enumeration studies, more than just simple presence/absence testing, are essential if we are to understand the ecology, distribution and ‘life cycle’ of these organisms. Once excreted into the environment at least a small proportion of the voided cells must adapt a suitable survival strategy until ingested by another susceptible host. Vehicles and vectors that transmit Campylobacter between hosts must play a significant role in the epidemiology of this organism. Although Campylobacter has been the most frequently isolated pathogen associated with gastrointestinal infection in England and Wales since 1981, its transmission to humans is poorly understood. Much has been learnt about the epidemiology of Salmonella from studying outbreaks. In turn, these data have informed control strategies that have no doubt played a part in the current downward trend in Salmonella cases in the UK. However, most cases of human campylobacteriosis are thought to be sporadic and it is frustrating that the application of most available molecular subtyping techniques (for review see Frost 2001) to resolving Campylobacter infections has, over the last decade, yielded more questions than answers. Population genetic analysis has recently revealed that C. jejuni is genetically diverse with a weakly clonal population structure and that intra‐ and inter‐species horizontal genetic exchanges are common (Dingle et al. 2001). It is widely held that the major source of sporadic cases is the handling and consumption of contaminated poultry meat and this is supported by case–control studies (Tauxe 1992). Broiler flocks are frequently contaminated with C. jejuni (see Corry and Abatay 2001 for review) as are raw poultry meat and its packaging at retail (Jorgensen et al. 2002). Many studies have shown that once Campylobacter is introduced into a broiler shed, birds rapidly excrete high numbers in their faeces and the organism spreads rapidly so that 100% of birds may be colonized within a few days. Avian species are purported to be the natural hosts of thermophilic campylobacters because they have a core temperature of 42°C, which is the optimum growth temperature of C. jejuni. The significance of Campylobacter colonization of dairy and beef cattle and sheep relates not only to the potential for contamination of milk at the farm and the carcass at slaughter, but also surface and sub‐surface water during disposal of abattoir effluents and animal slurries to land. Further, many studies have found the presence of farm animals, such as cattle and sheep, on broiler farms is associated with increased risk of infection in broiler flocks. The relative direct and indirect contributions of cattle and sheep to sporadic human infections are currently unknown (Frost 2001). There is little evidence to suggest that red meat is an important risk factor for human infection, either from case–controlled studies or prevalence studies on meat. This possibly reflects the more hygienic slaughter procedure for ruminants than poultry, although chilling and desiccation have a significant effect on survival of thermophilic campylobacters on the carcass (Grau 1991). Gross microbial contamination of the carcass with gut contents may occur during evisceration but it is thought that most contamination occurs during removal of the hide or from cross‐contamination from hide to carcass via hands and instruments of slaughtermen (Gannon 1999). Although rates on offal tend to be higher (Bolton et al. 1985), most, if not all, surveys over the last two decades have found that the incidence of Campylobacter on red meat is low compared with poultry meat even when other pathogens, such as Salmonella and Escherichia coli O157, can be isolated. An extensive survey of 1400 butchery products and premises isolated Campylobacter spp. from 15 of 2330 raw meat products, including four raw sausages, 10 raw burgers and one other, compared with 84 positive Salmonella and The prevalence on higher than Campylobacter is more frequently isolated from the than other et al. 2002) and contamination of offal at retail has been at et al. However, there is now a growing body of molecular subtyping evidence that suggests the significance of non‐poultry sources of human clinical infection has been et al. et al. et al. et al. 2001). studies have found that from poultry, cattle, sheep and humans are by a of molecular subtyping methods such as and In the et al. 2001 found that to have a host that only isolated from one host However, accounting for of in the had been isolated from cattle, sheep and faeces as well as human clinical This that cattle and sheep are colonized and excrete C. jejuni which are of disease in the community. have significant for two there has been to that or non‐poultry as an infection risk and it questions molecular subtyping and studies can understand the sources of sporadic human infection when from a range of potential sources are The role of ruminant animals in outbreaks is understood. from and milk for outbreaks the For the of Campylobacter enteritis in when contaminated water was the et al. Campylobacter jejuni was also isolated during the recent of coli associated with contaminated in the of 2002). The of to sub‐surface is recognized as outbreaks in the UK et al. and other countries have been associated with Campylobacter is most to in milk because of contamination but on outbreaks have been to Campylobacter which has high numbers of to be excreted into the milk et al. have a low incidence and of Campylobacter in UK milk and methods of However, consumption of raw milk was implicated in of outbreaks to the for in the between and et al. and four of outbreaks to the from England and Wales between and 1994 et al. of human infection with and In many countries there is a or summer et al. 2002) while in countries there is little variation there may be more infection during the 1992). number of studies have to the which in the UK occurs than the in Salmonella is also in the (Tauxe and other countries such as et al. but is a little in summer in and the is in of the including (Grau 1991) and to the seasonality of common source outbreaks of Campylobacter the national Campylobacter in the where outbreaks by raw milk or contaminated water have a distribution with in and data suggest that the and of outbreaks are from sporadic It was that the seasonality of human infections reflect important in the of the poultry and reservoirs of Thermophilic are isolated from the intestinal tract of ruminants although the rate between and flocks. the last two decades prevalence in adult cattle had been at in et al. in et al. in et al. in et al. 2001) and et al. 2000) in the such as size and of and isolation and have been to for For a high incidence of C. jejuni has been observed in cattle in compared with cattle on et al. Isolation rates between In the Campylobacter spp. isolated from and of and Corry et al. the Campylobacter isolation rate of cattle and sheep at a abattoir in over a from the small and for thermophilic campylobacters by a of direct of a free selective medium and also by of the in for direct Campylobacter was isolated from of cattle which compared with UK that and of adult cattle Campylobacter at slaughter (Bolton et al. and including an a of found to be Campylobacter positive a of et al. the isolation rate from was at by direct and by An has been found to increase the of Campylobacter from ruminant This may be because the average number of Campylobacter in adult and intestinal is lower than in broiler faeces yielded an average of which is to observed by found in In the studies of et al. the only one to numbers and the maximum was Campylobacter the low of C. jejuni cells this a risk if the meat should contaminated with contents during the slaughter intestinal yielded an average of Campylobacter and a significant trend was observed in the years of data which that the Campylobacter in while the was in et al. This with lambing and with outbreaks in young of Salmonella and et al. However, neither young nor should be among the at the In a trend was not found in the data from cattle at important factor affecting the in rate is the on intestinal observed in studies which faeces or The may an of recent shedding but may the rate of and et al. that more to Campylobacter than faeces from the and that this It also that a may not an animal is a or et al. not Campylobacter spp. from the or but C. jejuni isolated from the of of cattle and There is little published data to suggest that C. jejuni is able to grow or in the but its presence suggests recent (Grau 1991). An may increase the of infection in the lower intestinal tract in animals but the organism must the of adult animals if is to occur during an adult The that shedding of such as Campylobacter and coli are poorly understood. little data are available on pathogen shedding in colonized animals and more is to patterns of Such studies are to as they analysis of a number of The application of may the for analysis with a high of of Campylobacter and coli by colonized cattle is et al. et al. studies that a lower prevalence of Campylobacter is observed on the farm compared with at (Grau et al. 2002). survey on in of voided faeces from a Campylobacter positive dairy found that the 10 positive yielded but yielded between and C. jejuni This suggests that just a small proportion of a may be shedding high numbers of the organism at The of was recently by an environmental that an of coli associated with use of et al. 2002). that is animals shedding than may a risk at the abattoir and as in a or transmission contamination of their water or contaminated for when are excreted in higher numbers et al. 2002). Methods for rapidly animals that are shedding high numbers of are highly if such animals can be held from slaughter or from a or for a on four farms the variation in the numbers of Campylobacter in the faeces by the dairy numbers in dairy faeces lower than from intestinal of data over years revealed a that the in numbers from to the had two in and in on farms but on farms to the on farms by in and in studies have in Campylobacter rates within dairy in of both the and During a of two dairy in the of C. jejuni was isolated from of during the from neither during the but it during In and the isolation rate during and found high isolation rates in both summer and autumn but low in The that conditions in autumn of an summer and that these to The of the in the data over years that there is a The in the dairy not be with or maximum temperatures, of or et al. The in the data from farms to one another from farms only suggest that there may be temperature factors, for birds, or may be It is not in Campylobacter is to that in population of campylobacters, or The and autumn with milk and of which suggest that may a as these are in animals for beef et al. in shedding patterns may reflect in the gut flora. However, UK are to their dairy to the for milk and dairy The with the from to summer and the autumn to and may reflect a in or Seasonal patterns of shedding of other have been associated with The prevalence of in the faeces of dairy cattle is higher during the of than when animals are on 1990). during including and are the major sources of both pathogenic and species of 1990). For dairy cattle, of or and has been identified as a risk factor for shedding C. jejuni et al. 2000) but it was not that the was contaminated with the The of is by In the area a to as means that are on or high and to on lower before are for on lower until the lambing which is between and of Campylobacter shedding by sheep on farm and on farms in the revealed that the organism was on Campylobacter shedding was in and when sheep on and compared with when they (Jones et al. 1999). The rates of shedding with increased as a of and new in have also been to cause increased shedding of coli by sheep et al. of disease outbreaks in sheep can be observed lambing et al. et al. found that young on the farm are for Campylobacter which suggests that horizontal not transmission is the by which they infection. that not shedding Campylobacter before lambing shedding lambing while that low numbers before lambing of 100% of to either of from and that for had the et new rapidly the organism from the farm environment via horizontal transmission et al. In a of of calves, free of Campylobacter at but most shedding within days. numbers be found in within of more than campylobacters before they of until when the average had to between and which was to that by the dairy et al. of are in the of meat and the of which may of infection. In order to the of dairy are to than beef cattle. In with dairy it is common in the of beef cattle for to on of to have with their at and it is unlikely that they of of either via their contaminated or from food or water It is that animals in this are from their as well as from other sources and this may be in the high rates of the beef cattle at is about data from young between and is that the Campylobacter numbers in the faeces are to the high numbers observed in broiler before slaughter at of of the of animals may for variation in average Campylobacter numbers in cattle are to by the they to slaughter the average of the dairy is to be The average numbers of campylobacters in from to is between 10 and higher than found at the abattoir in of beef cattle at slaughter or the faeces of adult on C. jejuni from the of which was 10 higher than the average observed in adult cattle. rates and of Campylobacter infection have been observed in than in adult cattle, for (Grau and et al. average dairy of and beef 1991). dairy dairy will of faeces which in summer may be on and the farm when are for but during must be in (Jones 2001). Campylobacter jejuni was isolated from from farms in numbers between and et al. that there was little in et al. that the of C. jejuni was during of beef slurries which was more than 10 that of or to livestock of bacteria when farm was have now increased and frequently cattle may be on or from where the is and along with water and other on the farm may also be so that the contents of a may from farm to on may be in when or the in and on land. from is of by on land. et al. that slurries to in in summer campylobacters than slurries to in but that survival on in much than in Further, and the over rapidly in summer while in to a of contaminated runoff. The of as of campylobacters has been shown by et al. et al. that including can the of Campylobacter in poultry flocks. should be considered an important in both and to Campylobacter in It be that the gastrointestinal of young ruminants may allow colonization of Campylobacter or other It is not young calves, once excrete the or they with new their adult is it how of contaminated or water or to new the rate of Campylobacter shedding in adult only a few studies have in within dairy such data it is to devise a control et al. found among from adult dairy on four found that of adult animals a range of than of to C. jejuni by a single and of animals two only are to and molecular from isolation is an important part of such There are no that although studies have found that lower can species and to higher et al. which to increase the from a Campylobacter jejuni has been isolated from birds such as and that birds and be a source of new within flocks or Stored animal slurries and on potential pathogen vectors such as birds and and contaminated water and free birds which have been as potential of infection in poultry flocks 1992). and that 10 of with to water Campylobacter, at least while two that only water et al. also found lower rates during when they only water and higher isolation rates during summer when their source of water was a They isolated C. jejuni from most of the Using and they able to that the was contaminated by number 25 and that this was a transmission for infection of the of the also found that may excrete one et al. that contaminated water may be a transmission of coli within and water may be contaminated with Campylobacter spp. et al. et al. 2001). sources can from where the water is and may from farms or has been implicated as a source of in broiler farms although Campylobacter may not be et al. et al. Young cattle and sheep on the farm are to Campylobacter infection within the few of excrete high numbers of Campylobacter in their faeces when and cattle Campylobacter their This may a ruminants to slaughter in the of England one or more species of thermophilic Isolation should include an to fully the isolation Campylobacter is isolated from and of which may be by birds and Contamination of surface and sub‐surface may transmit Campylobacter within and between farms and other livestock and other animals on farms Campylobacter that are of disease in the community. ruminants animals play a significant role in the contamination cycle of understanding of the patterns of shedding by animals on the farm and the between environment and Campylobacter are in order to devise intervention if they are to be