A brief summary of the lifecycle of the parasite: larvated eggs are excreted in the faeces of the host - a dog. The embryonated eggs are ingested by the intermediate host - various species of coprophagous beetles, where they develop to infective L3 stage. Transport hosts such as lizards, frogs, birds and small mammals may eat the beetles, but the L3 remains infective. The dog will need to ingest either the beetle (coprophagia) or the transport host to become infected. Once in the stomach, the infective larvae penetrate the gastric mucosa, migrate within the walls of the gastric arteries to the abdominal aorta and from there to the thoracic aorta. Here the larvae mature to a subadult L4 phase over a period of 3 months. They then migrate through the wall of the aorta through the mediastinum to the oesophagus where they develop into a parasitic nodule over 2–3 months. The adult female will deposit her eggs into oesophageal lumen through an operculum in the nodule. Each nodule may contain numerous adult worms. Egg production is maximal from 9 month postinfection for several months.
Clinical signs exhibited can be attributed to three causes: response to or damage by migrating larvae, the presence of the oesophageal nodule and neoplastic transformation of the nodule.
Larval migration can cause immune-mediated polyarthritis, aortic aneurysm and rupture, rupture of other large thoracic blood vessel, mediastinitis, pyothorax or chylothorax and neurological spinal cord signs. Aberrant migration results in the development of parasitic nodules anywhere in the body. The oesophageal nodule will cause regurgitation due to oesophageal obstruction as well as hypersialosis and excessive dysphagia and odynophagia, especially in certain predisposed breeds (fox terrier types).1 Once neoplastic transformation has occurred, the patient will usually exhibit regurgitation, weight loss and sometimes hypertrophic osteopathy.
Based on the above clinical signs, which are generally quite dramatic, one may ask why diagnosis is such a challenge. The complications from larval migration are relatively rare, although quite catastrophic when they do occur. The nodule(s), especially in larger dogs, often can be quite asymptomatic, and these dogs will often only develop clinical signs once neoplastic transformation has occurred.
Diagnostic methods available include faecal flotation, radiographs and endoscopy as a good minimum data base. Ova will only be present after the pre-patent period, which in S. lupi is anything from 4–6 months. Even though the eggs are heavier than most helminth eggs, they are actually most easily visible with normal faecal flotation fluids, compared to other previously recommended solutions.2 The sensitivity of faecal flotation in the diagnosis spirocercosis is only about 67%: nodules may not have an operculum (immature); worms are not always laying eggs and most neoplastically transformed lesions no longer have worms present.2
Thoracic radiographs are easily accessible and very helpful with an 86% sensitivity and 100% specificity if all 3 following parameters are assessed. (1) The parasitic nodule is generally seen as a caudodorsal mediastinal mass with a smaller number being mid-dorsal, overlying the cardiac silhouette. Additional changes which are pathognomonic for spirocercosis are (2) aortic aneurysm and calcification of the aortic wall7 as well as (3) spondylitis of the ventral vertebral bodies of thoracic vertebrae T8–T11 (range T5–L1).5 Dorsoventral (DV) and right lateral recumbent (RLL) views are preferred, as they allow for improved visualisation of the descending aorta aneurysms and avoid misinterpreting the normal oesophagus in the LLR view as a mass.3
The sensitivity of radiographs as well as the amount of information gained is increased with inflation of the oesophagus with air as a negative contrast medium.6 Radiographic changes can also be used to help decide if there is neoplastic transformation or not. The mass length was not significantly different, but the height and width of the malignant masses was significantly greater (62 ± 16 mm and 74 ± 21 mm) than the benign group (46 ± 23 mm and 49 ± 26 mm, p < 0.006).4 There is, however, a large overlap. The length of the mass is not reliable, as there are often multiple nodules in the oesophagus and this causes summation along the long axis.
Spondylitis was more prevalent in the malignant group: 68% vs. 39%. Pulmonary metastases and hypertrophic osteopathy indicate malignancy.4 Patients with malignancy are generally older (6.4 ± 1.9 years) than those with early parasitic nodules (4.93 ± 2.8) and are also more significantly anaemic (0.34 vs. 0.41%), have a neutrophilia (26.06 vs. 12.23 x 109/ml) and show weight loss.4
Using the clinical, laboratory and the radiographic picture, a reasonably reliable diagnosis or malignant spirocercosis can be made.
Diagnosis can only really be confirmed, however, by endoscopy and biopsy. Oesophageal nodules are also not always projecting into the oesophageal lumen; rarely they may protrude from the serosal surface and results in a negative endoscopic exam. The typical parasitic nodule is visualised in the caudal third of the oesophagus. Some nodules may occur in the stomach (< 10%). Very early lesions appear to be a reddened area like burst veins on the mucosa, early lesions are a pink mound/hillock, and mature lesions are a pink mound in the oesophageal wall with a pink nipplelike tip (operculum) through which the worm deposits its eggs. Neoplastic transformation causes a cauliflower-like appearance of the nodule, which develops a more pedunculated shape with mucosal ulceration and necrosis. The mass is often greenish grey in colour, is friable, bleeds easily and the dog's breath smells foul.
Biopsy of these masses has to reach beyond the necrotic tissue to get to a representative sample of tissue. Endoscopic biopsy forceps are small, so multiple stack biopsies through the same hole are taken. These biopsies may yield a false negative result. If I see the typical macroscopic changes, I consider the diagnosis made. False negative biopsies can also be made in relatively benign-looking nodules, as neoplastic transformation initially starts centrally in the nodule - this is uncommon and would present as a nodule which does not regress as typically expected with treatment.
If a neoplastic nodule is diagnosed or suspected, and surgery is an option, a CT exam is requested to determine the extent of the malignancy and decide if it is in fact operable. The neoplasm may extend through the oesophageal wall and involve structures within the mediastinum. Alternatively, despite having a large mass effect, some of these tumours are actually very pedunculated, which makes them amenable to surgery.
Further research has been conducted to try and reliably and less invasively differentiate benign and malignant canine spirocercosis: IL 8 is elevated in malignancy; TEG showed neoplastic cases were hypercoagulable;13 Serum vascular endothelial growth factor (VEGF) was significantly increased in neoplasia;11 plasma ALP levels and CRP did not differentiate; vitamin D levels were decreased in neoplastic cases.12
Uncomplicated canine spirocercosis is treated using the macrocyclic lactones. A variety of regimens using doramectin (extra-label) have been effective. The exact effective/minimum dosage and frequency is unknown and a standard dosage of 400 ug/kg is used either weekly or every second week. The doramectin in either injected but can also be given orally (unpublished data), for 6–12 weeks. Monitoring is by radiographs or endoscopy. The problem with deciding when the patient is cured is that we only measure response to therapy indirectly. The nodule is not a granuloma as previously thought but a proliferation of fibroblasts with a mixed, mainly neutrophilic and lymphocytic, inflammatory response. The time it takes for this nodule to regress is not necessarily an indication of the continued presence of a live worm. If the nodule is regressing by 6–8 weeks, I stop therapy and start preventative therapy; others continue treating until the nodule has completely regressed.
Milbemycin oxime (Milbemax®) is effective in the prevention of canine oesophageal spirocercosis at minimum dose of 0.5 mg/kg, monthly, starting at 2 weeks of age.8 In these animals from endemic areas, there was evidence of aortic aneurysms and scarring, indicating that the animals had in fact become infected, but only 10% of animals had any evidence of oesophageal nodules and only one nodule in each animal was found compared to between 1–4 nodules in control animals. Milbemycin oxime was also evaluated as a treatment - starting with a single dose 30 days post experimental infection.9 In this trial, a single treatment (0.5 mg/kg) was 79% effective in preventing establishment in the oesophagus, although the thoracic aorta did show parasite-induced damage similar to that of the untreated controls. In animals where the dose was repeated either monthly or weekly, there were no oesophageal lesions, but these numbers were very small. What this trail also clearly showed was that most dogs vomit severely within the first hour of experimental infection, but larvae were not present in the vomitus. This leads to the assumption that migration through the gastric mucosa causes emesis.
Imidacloprid 10%/moxidectin 2.5% (Advocate®) spot on treatment has also shown efficacy against canine spirocercosis, both as a preventative (no lesions in aorta of 7/8 dogs and no oesophageal lesions in 8/8 dogs) as well as a treatment (weekly) in experimentally infected dogs starting at d 170 post infection - oesophageal nodules in 3/8 dogs, of which one contained no live worms.10
Both Advocate® and Milbemax® are safe to use in dogs susceptible to ivermectin toxicity due to MDR-gene defects.
Eradication of the parasite in the environment is unlikely. Dogs, as the final host, are responsible for contaminating the environment. The beetles responsible for harbouring the parasite are the small beetles which live in the soil and burrow into the faeces, not those that roll balls of faecal material. Frequent collection of faeces not only keeps substrate to minimum, it also prevents infection due to coprophagia. Transport hosts keep the infection patent, but do not cause environmental contamination, as the larvae are encysted within their musculature, they have to be eaten by the final host which passes eggs with faeces.
1. Van der Merwe L, Christie J, Clift S, et al. Salivary gland enlargement and sialorrhoea in dogs with spirocercosis: a retrospective and prospective study of 298 cases. J S Afr Vet Assoc. 2012;83(1):920–922.
2. Christie J, Schwan E, Bodenstein L, et al. The sensitivity of direct faecal examination, direct faecal flotation, modified centrifugal faecal flotation and centrifugal sedimentation/flotation in the diagnosis of canine spirocercosis. J S Afr Vet Assoc. 2011;82(2):71–75.
3. Kirberger R, Dvir E, van der Merwe L. The effect of positioning on the radiographic appearance of caudodorsal mediastinal masses in the dog. Vet Radiol Ultrasound. 2009;5(6):630–634.
4. Dvir E, Kirberger R, Mukorera V, et al. Clinical differentiation between dogs with benign and malignant spirocercosis. Vet Parasitol. 2008;155:80–88.
5. Kirberger R, Clift S, van Wilpe E, et al. Spirocerca lupi-associated change vertebral changes: a radiologic-pathologic study. Vet Parasitol. 2013;195:87–94.
6. Kirberger R, Van der Merwe L, Dvir E. Pneumoesophagography and the appearance of masses in the caudal portion of the oesophagus in dogs with spirocercosis. J am Vet Med Assoc. 2012;240(4):420–426.
7. Kirberger R, Stander N, Cassel N, et al. Computed tomographic and radiographic characteristics of aortic lesions in 42 dogs with spirocercosis. Vet Radiol Ultrasound. 2013;54(3):212–222.
8. Kok D, Schencker R, Archer N, et al. The efficacy of milbemycin oxime against pre-adult Spirocerca lupi in experimentally infected dogs. Vet Parasitol. 2011;177:111–118.
9. Kok D, Williams E, Schenker R, et al. The use of milbemycin oxime in a prophylactic anthelmintic programme to protect puppies, raised in an endemic area, against infection with Spirocerca lupi. Vet Parastiol. 2010;174:277–284.
10. Austin C, Kok D, Crafford D, et al. The efficacy of topically applied imidacloprid 10%/moxidectin 2.5% formulation (Advocate®, Advantage® Multi, Bayer) against immature and adult Spirocerca worms in experimentally infected dogs. Parasitol Res. 2013;112:S91–S108.
11. Mukorera V, Kirberger R, Mateba P, et al. Vascular endothelial growth factor concentrations in dogs with spirocercosis. J Vet Intern Med. 2013;27(6):273–276.
12. Rosa C, Schoeman J, Berry J, et al. Hypovitaminosis in dogs with spirocercosis. J Vet Intern Med. 2013;27(5):1159–1164.
13. Pazzi P, Goddard A, Kristensen A, et al. Evaluation of hemostatic abnormalities in canine spirocercosis and its association with systemic inflammation. J Vet Intern Med. 2014;28(1):21–29.