Box 1 | What is a super-shedder?

Super-shedders or super-spreaders?

The terms super-shedding and super-spreading are not always clearly distinguished in the literature and we therefore recommend the following definitions.

Super-shedder. An individual who for a period yields many more infectious organisms of a particular type than most other individuals of the same host species. Typically, many more infectious units are released from a super-shedder. The term is most useful when there is a clear biological basis for the distinction between super-shedders and non-super-shedders (such as host genetic differences, host immune suppression, type differences in the infectious organism, or the presence or absence of co-infections).

Super-spreader. An individual who has more opportunities to infect other hosts with a given pathogen type than most other individuals of the same host type. Typically, such an individual has many more contacts — defined by the route of transmission of the pathogen (for example, direct contact through proximity, physical contact or sexual contact, or indirect contact through contaminated food or bites from a large number of vectors)⁵⁸.

Super-shedding and super-spreading are independent traits: super-shedding reflects the interaction of the host with the pathogen, whereas super-spreading reflects the interaction of the host with other hosts.

Escherichia coliO157 super-shedders

For E. coli O157, several working definitions of a super-shedder can be found in the literature. The most basic of these are derived from single direct counts of E. coli O157 in faecal samples. Suggested cut-offs for super-shedding are counts of 10³ or 10⁴ colony forming units (CFU) per gram of faeces^{15, 17, 59, 60} or the simple identification of outlying counts⁶¹.

Such measures are simple to use but do not directly indicate whether an animal is colonized at the terminal rectum, nor do they allow for (possibly substantial) sample-to-sample variation in bacteria counts during the course of an infection. A recent longitudinal study²⁰ that used recto–anal mucosal swabs (RAMS) defined a super-shedder on the basis of both mean concentration (10⁴ CFU) and persistent colonization (4 consecutive positive RAMS, for samples taken twice per week for 14 weeks).

This definition seems to be ideal, as it encompasses both properties of a super-shedder: high excretion and colonization of the terminal rectum. However, longitudinal examination is not always possible. For the purpose of identifying super-shedders (for control purposes, for example) we therefore need a suitable working definition that can be readily used in field situations. A recent study²⁰ that observed the concentration of E. coli O157 in faeces was positively associated with the estimated duration of culture-positive status. This is consistent with the findings of a study of cattle at slaughter in which shedding of >10³ CFU per gram of faeces was associated with bacterial carriage close to the terminal rectum, whereas shedding of <10³ was not¹⁷.

A more formal analysis of E. coli O157 faecal counts was performed in a recent paper, in which mixture distribution analysis suggested a cut-off of 3,135 CFU per gram of faeces (with low and high confidence thresholds of 1,658 and 10,395, respectively)¹³ (Fig. 3). This figure confirms the approximated estimates of >10³ to >10⁴ in other literature.

On the basis of the available evidence, we propose a working definition of an E. coli O157 super-shedder as an animal that excretes >10⁴ CFU per gram of faeces. Although less stringent than previous recommendations¹⁹, we consider that such high shedding levels are unlikely to occur without colonization. We note, however, that at times during the course of infection, or owing to sampling variation, even colonized animals may excrete at levels below this threshold. In other words, our working definition has high specificity, but somewhat lower sensitivity for detecting super-shedders.

It is also possible that wildlife reservoirs and other livestock species play a part, as sheep have been reported to excrete similar concentrations of bacteria to super-shedding cattle²⁴. In a study of sheep at slaughter in Scotland, the counts of E. coli O157 in faeces were occasionally >10⁷ CFU per ml, which suggests that other host species are also super-shedders of the organism (M.C.-T., D.G., C.L., L.M. and M.W., unpublished observations). In addition, a high prevalence of E. coli O157 was observed²⁴ in a sheep flock in Scotland, with individuals in the flock shedding up to 10⁶ CFU per gram of faeces.