CASE NOTES
Gongylonemiasis causing oral ulceration (with exclusion of vesicular disease) in merino ewes from Barossa Valley, South Australia
Dr Catherine Harper, Barossa Veterinary Service, 29 Railway Terrace, Nuriootpa SA 5355 and 32 Mildred Street, Kapunda SA 5373
Dr Daren Hanshaw, Gribbles Veterinary Pathology
Posted Flock & Herd May 2019
Introduction
Mouth lesions and ulcerations have been detected in sheep at routine inspections from time to time. Differential diagnoses for such lesions include some serious exotic diseases such as foot-and-mouth disease and Bluetongue. A study in Victoria (DPI Victoria 2006) described 27 different conditions that were mainly ulcerations or nodules, but lesions on the tongue of sheep are reported rarely.
In this case, a producer reported that one of his three mobs of Merino ewes with lambs at foot were “frothing at the mouth”, one ewe had died and approximately 20 percent of the flock were affected. The producer was concerned about losing more animals and requested an investigation. Since serious exotic diseases were a possibility, the Department of Primary Industries and Regions, South Australia (PIRSA) subsidised the investigation and laboratory costs.
Serious exotic diseases were ruled out and a diagnosis made of an unusual parasite - Gongylonema spp. The affected ewes appeared to improve after treatment with antibiotics and an anthelmintic drench, and no further cases were reported.
History
An experienced sheep producer contacted the primary author in late June 2018 to report that he had noticed sheep frothing at mouth the day before. Approximately 40/240 three-year-old ewes with lambs at foot were affected and occasional cases in two other mobs of ewes were seen. The ewes had been vaccinated for enterotoxemia, tetanus and caseous lymphadenitis (commonly known as “3-in-1”e.g.Glanvac® 3 - Zoetis) prior to joining, and possibly treated for internal parasites with an oral ivermectin drench. The affected ewes were in poorer body condition than other ewes, and had white froth and saliva dripping from the mouth. The sheep were being fed some barley as a trail feed with some supplementary hay, and pasture was of poor quality and fairly short with moderate faecal contamination. No obvious weeds, toxins or heavy metal contamination was apparent and there was plentiful water available.
Image 1. Heavily grazed pasture.
Ten affected ewes were examined, all were bright and alert but were in poor body condition (1-2/5), with a mild pyrexia (39.3-40.1°C), and white frothy salivation. There were no respiratory signs or coughing. One sheep had multifocal coalescing yellow adhesions across the tongue but all others tongues were normal with no evidence of blisters, wounds or similar lesions.No lameness, inflammation of the feet, interdigital lesions, or coronary band lesions were observed. One sheep was sacrificed for a full post-mortem examination and a full range of samples submitted. There were no gross lesions on the tongue, oesophagus or abomasum of this animal and no parasites observed in intestines.
Image 2. A salivating, unhappy ewe.
The most severely affected individual sheep were treated with 'Alamycin' 1ml/10kg bodyweight (oxytetracycline, 300 mg/mL, Norbrook Laboratories) and 'Metacam' 1ml/20kg bodyweight (meloxicam, 20mg/mL, Boehringer Ingelheim) and faeces for a faecal egg count were collected. The producer was advised to move the sheep to a fresh paddock and offer hay in addition to barley as a way to minimise risk of acidosis as a potential cause.
The producer drenched all sheep with 'Cydectin' at a rate of 1ml/5kg bodyweight (moxidectin, 1g/mL, Virbac Australia). The affected sheep appeared to recover, and there were no further cases reported.
Results from Laboratory tests
The final diagnosis based on histopathology was gongylonemiasis. Foot-and-mouth disease, vesicular stomatitis and Bluetongue were excluded in samples sent to the Australian Animal Health Laboratory (AAHL). Further detail from the report is quoted below:
“The most significant findings are seen within the tongue and oesophagus of this sheep: there is evidence of a mucosal hyperplasia, parakeratosis, erosion and ulceration and mixed neutrophilic (suppurative) and eosinophilic inflammation associated with numerous nematode parasites that are burrowing through the mucosal squamous epithelium. This is likely to represent a severe infection with Gongylonema spp.
Image 3. Cross section of worms seen in tongue tissue.
Gongylonema is a rare spirurid nematode parasite of sheep and goats (and various other mammalian species) found worldwide. G. pulchrum worm is found within the tissues of the oesophagus, where the parasite burrows through the cornified layer of the mucosa forming serpiginous tracks. The worm has an indirect life cycle, with dung beetles or other insects (e.g. cockroaches) acting as intermediate hosts. The final host becomes infected when ingesting carrier beetles or directly (e.g. on pasture), or indirectly through contaminated feed. This parasite is normally an incidental finding and of little clinical significance. I have occasionally seen one or two worms as an incidental finding in the oesophagus of ruminants, without any obvious inflammatory response. However, in this case, there are large numbers of worms within the epithelium and their presence is clearly provoking a severe inflammatory reaction, complicated by secondary bacterial infection.
It could be that there is a hypersensitivity reaction stimulated by parasite migration through the mucosa. The upper alimentary lesions are presumably responsible for the hypersalivation and perhaps the poor condition (e.g. pain associated with feeding or swallowing?) Mild pyrexia might be due to the secondary bacterial infection.”
The faecal worm egg count was low - 185 eggs per gram.
Interpretation
This case is most unusual and it is difficult to find reported cases of clinical disease attributable to infection with this parasite in the Australian literature. Nieberle & Cohrs (1966) describe G. pulchrum as “a whitish threadlike filarial worm 4-14.5 cm long found free in the oesophagus or coiled in the epithelium, apparently without causing any disturbances”. References from Iran describing experimental infection report that mild inflammation may occur on the tongue and oesophagus approximately 10 days following ingestion.
Discussion
This clinical signs seen in this case could well have been caused by an emerging or exotic disease, and oral lesions in sheep are very rarely reported in SA.
Occasionally producers report cases of “vomiting sheep” where a greenish liquid is seen dribbling from the mouth, and under investigation this may result from poor dentition, foreign bodies, drenching injuries, or acidosis. However, in this case obvious and dramatic symptoms were observed and it is comforting that the producer sought professional advice immediately.
Seasonal conditions in SA had been dry leading to reduced pasture growth in autumn and winter, an important contributor to nutritional stress in livestock. In this case, ewes under maximum nutritional demand may have been grazing closer to the ground and consuming intermediate hosts (dung beetlesetc. or larvae directly), where in better seasons they may not have.
Treatment of the affected sheep with antibiotics, an anti-inflammatory, and anthelmintics appears to have been effective in this case.
References
- Eslami A., Study on the Prevalence and Pathology of Gonglyonema pulchrum (Gullet Worm) of Sheep from Iran. Global Veterinarian 2010 5(1): 45-48
- Nieberle & Cohrs (1966), Textbook of the special anatomy of domestic animals, Pergamon Press
- Department of Primary Industries, Victoria (2006), “Ovine mouth pathology”
