In April 2004, several horse studs in the Hunter Valley of New South Wales suffered significant numbers of unusual abortions in mares of mid-gestation. The presenting signs included amnionitis and funisitis with inflammatory changes extending into the allantoic surface of the allantochorion in chronic cases. In some cases chorion was also involved. Bacteria of enteric and environmental origin, normally not pathogenic in the horse, were isolated from the aborted foetuses. The condition was characterised and termed Equine Amnionitis and Foetal Loss (EAFL). The clinical and pathological features of EAFL are similar to Mare Reproductive Loss Syndrome (MRLS), a condition that occurred in Kentucky, USA, in 2001. The exoskeleton of the Eastern Tent caterpillar (ETC; Malacosoma americanum) was identified as the causative agent and setae (hairs) were suggested to be part of the aetiology of the syndrome. The ETC does not occur in Australia but a number of other caterpillar species that have external setae similar to the ETC do. One of these, the Processionary Caterpillar (Ochrogaster lunifer), was identified in areas where EAFL occurred.
Experiments were undertaken to investigate the role of Processionary Caterpillars (PC) in the aetiology of EAFL. In the initial study, pregnant mares in mid-gestation were gavaged with a slurry of 100 g whole PC daily for five days or until mares aborted, whichever occurred first. Three of the four treated mares aborted within 11 days of first treatment and the remaining treated mare was euthanased while her foetus was still alive. Samples for bacteriology and histopathology were collected from all four foetuses and the findings reflected those of clinical cases of EAFL. The second experiment, also using mares in mid-gestation, investigated shed PC exoskeleton as the possible abortigenic agent. At the time of collecting PC, the exoskeleton that had been shed into the nests at successive moults was collected and stored. Graded doses of shed PC exoskeleton (1 g, 2 g and 5 g) were administered to treated mares (n=3 per dose) daily for five days or until abortion, whichever occurred first. Abortions occurred in mares in each treatment group with a greater tendency for acute abortion in mares receiving higher doses. One mare from the 1 g treatment group aborted her foal 67 days after treatment. This abortion was similar to the chronic cases of EAFL. Other abnormal outcomes of pregnancy occurred in treated mares, with only one mare from each of the lower treatment groups delivering a normal foal. Bacteriological and pathological findings again reflected those of the clinical cases of EAFL. Some mares showed a transient urticarial reaction following the administration of PC or PC exoskeleton. Similar to clinical cases of EAFL, the mares in these experiments showed no outward signs of impending abortion.
The third and fourth experiments in this study investigated the effect of administration of shed PC exoskeleton to mares in the pre-placentation and the early placentation stages of gestation. In each experiment, six mares were administered 5 g shed PC exoskeleton daily for five days. Mares in the pre-placentation experiment were treated from gestation day 25 (GD25) and in the early placentation experiment, treatment started from GD46–GD51. One mare aborted in the pre-placentation experiment and two mares aborted in the early placentation experiment. Bacteria isolated were consistent with those described in EAFL. The ultrasonographic findings of the early placentation experiment were consistent with those described in cases of MRLS early foetal loss. An unexpected outcome from these studies was the occurrence of a case of focal mucoid placentitis in one mare from each of the pre-placentation and early placentation experiments. This is the first time that focal mucoid placentitis has been induced experimentally and provides an aetiology for this and the pathologically similar nocardioform placentitis. In all four experiments foetal death preceded any decrease in either progesterone or oestrogen.
The final experiment investigated the effect of repeat exposure to PC of mid-gestation mares that had previously experienced an experimentally induced EAFL abortion. The results of this study indicate that previous exposure to PC does not stimulate an immune response sufficient to protect the mare from EAFL in subsequent pregnancies. Histopathology performed on treated mares euthanased in this study has shown that the setae of the caterpillars can penetrate the gut wall and migrate to other tissues including the uterus and placenta. This provides a mechanism by which bacteria can be translocated from the gastrointestinal tract to the uteroplacental tissues.
The results of this project provide compelling evidence that Processionary caterpillars cause EAFL, and justify efforts to control exposure of pregnant mares to these caterpillars. The present studies have highlighted the complexities of investigating foetal loss in the mare. It is likely that the wide range of clinical presentations seen in EAFL reflects a combination of factors that come together to result in this condition.