Equine Amnionitis and Foetal Loss (EAFL) was first described in 2004 following an outbreak of abortions in mares that had an unusual and consistent pattern of clinical and pathological signs. Examination of reports for all equine abortion cases that involved submission of diagnostic material to the Scone Veterinary Diagnostic Laboratory between March and October 2004 indicated that EAFL was the most common identified cause, responsible for 28 (37%) of 76 cases (Todhunter et al., 2009). The case definition for EAFL (Todhunter et al., 2009) has similarities to descriptions of abortions associated with Mare Reproductive Loss Syndrome (MRLS) reported in Kentucky, USA in 2001 and 2002 (Perkins et al., 2007). MRLS has been shown experimentally to be associated with exposure of pregnant mares to Eastern Tent caterpillars (Malacosoma americanum; Webb et al., 2004). A similar hairy caterpillar, Ochrogaster lunifer (Processionary caterpillar; PC), was present in large numbers on several farms where EAFL abortions were diagnosed.
Experimental induction of EAFL: A series of experiments were conducted to determine the possible role of PC as an abortifacient in mares. The initial experiments were designed to simulate the situation in the field where most EAFL cases occur in mid to late gestation. The results showed that exposure of mares to preparations of either whole PC or shed PC exoskeleton can induce pregnancy loss (Cawdell-Smith et al., 2007). Gross pathology and bacteriology results were similar to those seen in field cases of EAFL (Todhunter et al., 2008). Of additional interest was the finding that some showed gross pathology that was very similar to that of Nocardioform placentitis (Cawdell-Smith et al., 2010).
It is well recognised that PC can cause an intense allergic reaction in humans. In the experimental studies, some but not all mares displayed a transient urticarial reaction following exposure to PC. In the studies using exoskeleton preparations, urticaria was not a predominant sign, although it did occur in some mares (Cawdell-Smith and Bryden, 2009). The mares exposed to exoskeleton preparations showed no detectible clinical abnormalities. A number of the abortions in these mares were acute but other outcomes were abortion with placental and foetal finding consistent with chronic infection as well as delivery of live but affected foals. In these cases, findings indicate that the initial insult occurred some time prior to abortion or birth.
The other distinctive feature of the field syndrome (Todhunter et al., 2009), and also observed in the experiments (Cawdell-Smith and Bryden, 2009), was the type of bacteria isolated from aborted foetuses. The range of organisms found was similar in both the experiments and in field cases. The organisms were common environmental or intestinal bacteria that are not normally associated with illness in horses. Although there were changes in haematology in some mares that were suggestive of a mild infection, those findings were not consistent. The isolation of bacteria and the pathology of the foetus and placenta were consistent with infection in the foeto-placental unit. This finding supported the conclusion that abortion occurs following passage of normal gut and environmental bacteria through the gut wall into the mare's blood stream, and then via haematogenous spread to the foetus.
The occurrence of mid-term abortions coincides with the migratory behaviour of PC and it was of interest to determine if these caterpillars could also cause either early embryonic loss (<35 days gestation), or abortion in mares from 45 - 60 days of gestation (Cawdell-Smith et al., 2008). While one treated mare did abort in the early embryonic loss trial, the result was inconclusive. However, it was shown that mares exposed to PC exoskeleton during the early foetal stage (45 - 60 days gestation) may abort.
Caterpillar exposure and possible mechanism of action: The studies described above demonstrate that exposure of pregnant mares to PC can induce foetal loss. However, it is well known that horses are able to sift through feed to avoid eating material that they do not wish to ingest. It is unlikely that horses would consume whole caterpillars. However, it is likely that as shed exoskeleton is extremely light (one exoskeleton weighs approximately 0.01g) and is easily blown around the pasture, it would be difficult for it to be separated from pasture by grazing mares.
It would appear from our results that structural elements of the caterpillars' body, more specifically those associated with the exoskeleton, or a compound in the caterpillar , or a combination of the two, allows the transfer of bacteria across the mare's gastrointestinal wall and the placenta. The resulting infection in the foetus leads to foetal death and then abortion. The PC species have hairs or setae that are barbed and it was thought possible that ingested setae penetrate the gut wall. This has recently been demonstrated in mares intubated with PC (Todhunter et al., 2010). The question then arises as to how easily bacteria cross the gut wall and the placenta. These caterpillars may also contain a toxin(s), which is consistent with their uticarial action, that may affect the gut and placenta and facilitate transfer of bacteria.
In conclusion, examinations are currently being conducted of histopathological changes in maternal, placental and foetal tissue samples from mares that have been treated with PC in an attempt to better understand the role of setae and/or toxins in the pathogenesis of EAFL. A laboratory animal model of EAFL is also being explored as an efficient alternative to using pregnant mares to allow detailed, ongoing studies of this condition. Moreover, there is justification for further studies that seek a greater understanding of the life cycle and population dynamics of processionary caterpillars, and of the caterpillar-associated factor(s) that induce abortion in mares.
Studies by the authors were funded by the RIRDC Horse Program and the Hunter Valley Equine Research Centre.
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This presentation was given at the Australian Equine Science Symposium in 2010. Engormix.com thanks the authors and the organizing committee for this contribution.