The case described here occurred in an outdoor fattening farm with 680 Gascon pigs in the Hautes-Pyrenees department of France. Every 2 or 3 months, 85 animals weighing approximately 30-40 kg arrive from a breeding farm and remain on the same plot until they are approximately a year old with an average carcass weight of 140 kg. The plot will then be subjected to a 2-month period with no pigs present on it. Eight batches are present simultaneously. The animals are fed with triticale flour in addition to what they find in the environment: acorns, chestnuts, grass, brambles, heather and elements from the soil excavation. Watering is provided by well water, which does not undergo any chemical treatment. To prevent parasites, the farmer adds Panacur 4%® to the drinking water at a dosage of 12.5 g per 100 kg of body weight every two months. Biosecurity is limited (there is no electric fencing, but wires are present).
In October 2019, the farmer noticed a loss of body condition and a loss of appetite in approximately ten pigs from a single plot. Breathing difficulties with an open mouth and complaints were observed in many animals, as well as nervous system signs that manifested as a wobbling gait. There was no diarrhoea. Two pigs that died suddenly were brought for necropsy to the Veterinary School of Toulouse. One pig had been found dead three weeks before this. These animals came from the same batch of 85 animals and were grazed on 4 hectare plot of land being used for the first time.
The clinical signs reported by the breeder were partially non-specific, with signs of weight loss and loss of appetite, but this suggests a less acute evolution than the sudden mortality reported concomitantly. Nervous system symptoms suggested central nervous damage that might have been caused by a wide variety of aetiologies, both infectious (oedema disease) and non-infectious (nutritional deficiency or intoxication). The respiratory symptoms may have also had various causes and may or may not have been related to the nervous system symptoms. Parasites can also lead to death and are important to consider in particular in an outdoor setting, such as metastrongias (Metastrongylus aprii) or trichurias (Trichuris suis), for example. However, since the plot on which the pigs were located was being used for the first time for fattening and since parasite treatment was administered regularly, this hypothesis was not retained at first.
Epidemiologically, the phenomenon appeared that it could be contagious or anazootic. Since it was limited to a single batch at the time of the call, with a 15% morbidity, 3.5% mortality and 23% lethality, a contagious origin was not retained as first. However, given the context of African swine fever in Europe, particular attention was paid not to overlook the possible detection of this disease, especially as biosecurity was not optimal in this outdoor farm and the wild boar population is increasing in the region [20].
Post-mortem investigation
Two pigs that were found dead were submitted for complete necropsy: an 8 month-old, 89 kg sow and an 8 month-old, 59 kg male pig that died the day before. On the sow, external examination presented congestive ocular and oral mucosa. Cavity openings revealed 500 mL and 15 mL yellow translucent effusion consistent with transudate in the peritoneal and pericardial cavities, respectively. The lung presented a moderate cranio-ventral consolidation and marked diffuse interlobular oedema (Figure 1).
The mediastinal lymph nodes were enlarged 2.5 x 1 cm and 3.5 x 1 cm. Extensive fundic congestion (Figure 2), as well as foamy liquid in the tracheal lumen and diffuse petechiae on the diaphragm, was found.
On the male pig, gross lesions were limited to 70 mL of yellow pericardial effusion, diffuse fundic congestion and multifocal foci of congestion in the caecal mucosa without luminal abnormalities. The rest of the examined organs were within normal limits, including the gross external examination of the brain and meninges.
The necropsic examinations did not reveal any specific lesions supporting a definitive diagnosis of an infectious agent except for in the lung, where there were the lesions might have suggested enzootic bronchopneumonia (Mycoplasma hyopneumoniae), and an underlying acute diffuse inflammatory lesion that did not allow the complete ruling out of a parasitic or viral interstitial pneumonia. At the time of necropsy, the brain, liver, and heart of both animals and the lung, kidney, mediastinal and mesenteric lymph nodes of the sow were harvested and fixed in 10% buffered formalin. After fixation, they are routinely processed in paraffin blocks, sectioned in 4 µm slices and stained with haematoxylin and eosin (HE) for microscopic evaluation.
At the same time, the farmer was contacted again to gather more information on the environment in which the animals evolved, in particular, on the possible neighbourhood issues and the plants present on the plot, bearing in mind that it was being used for the first time for pig fattening and considering the presence of nervous system signs, as well as the absence of clinical signs in the other groups present on the farm, all of which were on plots that had already been used for pig farming.
This second in-depth interview with the breeder revealed the significant presence of great eagle fern (Pteridium aquilinum) in the stockyard, which was confirmed by pictures sent by the breeder (Figure 3).
At that point, the lack of specificity of the necropsic findings associated with the presence of the fern without any change in the animals' management, particularly regarding the feed distributed, led to a strong suspicion of plant intoxication by this fern, which can lead to thiamine deficiency.
Histology
Samples taken from the male pig showed no abnormalities except in the brain. Lesions consisted of segmental cortical laminar and multifocal lesions in the brainstem, basal nuclei, and cerebellum, associated with acidophilic neuronal necrosis and spongiosis and admixed with gitter cell infiltration (Figure 4). Inflammation was observed in the leptomeninges and perivascular spaces, including endothelial activation, hyperaemia, and mixed leukocytic infiltration including mononuclear cells and eosinophils. Vascular fibrinoid necrosis and haemorrhages were occasionally seen. A diagnosis of polioencephalomalacia was assessed, suggesting a toxic or metabolic aetiology, including a toxic plant or a thiamine deficiency.
In the sow, the brain, lymph nodes, liver and kidneys were within normal limits. The heart showed lesions consistent with severe progressive polyphasic necrotizing myocarditis with mixed leukocytic infiltration, and the lungs showed leukocytoclastic necrotizing vasculitis with diffuse congestive and oedematous pneumonia (Figure 5).
A systemic infectious origin, notably viral, such as porcine circovirus type 2 (PCV2), was suggested without evidence of pathognomonic lesions, such as basophilic inclusions or granulomatous inflammation, and with myocardial lesions being found more often in runts or small piglets. Despite the nonspecificity, intoxication could not be ruled out, since pulmonary vasculitis was previously described in bracken fern intoxication of pigs [16].
Diagnostic and recommendations
Considering anamnesis, epidemiology, and post-mortem investigations and histology, the most likely diagnostic hypothesis retained was intoxication by great eagle fern. This was confirmed by the good response to the therapy that was implemented.
In the short term, it was recommended to prevent access of the animals to the eagle fern by changing their pasture or by removing the plants. Vitamin B1 was administered in the feed in the amount of 1 mL per 10 kg body weight for two days (Ultra B®: 4.46 mg thiamine and 2.06 mg pyridoxine (vitamin B6) per kg body weight per day). A remarkable remission was observed, allowing 6 of the 12 intoxicated animals with symptoms to survive (therapeutic success rate: 50%), but this did not compensate for the loss of initial body condition. In total, out of the 85 animals in the batch following this intoxication, 6 animals died and 6 recovered.