Our study showed that S. lupi is present in the black-backed jackal population in South Africa based on the microsatellite data as well as macroscopic and microscopic findings. The molecular study indicated a close relationship between the S. lupi found in dogs and jackals in South Africa. This was illustrated by the amplification of all nine loci in larvae collected from jackals similar to the dog-derived S. lupi, with the same levels of polymorphism that were observed as for dogs, where the allele size ranges of the jackal-derived samples fell within the range that was found for dog-derived samples for most loci. The nematodes found in most of the previous studies involving wild carnivores were not molecularly characterized. However, Spirocerca species isolated from gastric nodules in a red fox in Denmark was genetically distinct by 7 to 9% from isolates of S. lupi from Africa, Europe and Asia, and the authors suggested the existence of a cryptic species within Spirocerca .
The limitations of this study included the short duration of the study, the relatively small number of animals with S. lupi-associated lesions and the possibility that samples were not representative of all jackals, since culls were not randomly selected. This should be addressed in future research. Despite these limitations however, significant data were obtained in this study, namely the genetic classification of S. lupi and the presence of S. lupi-induced lesions in 16 of 93 jackals. The fact that there was no completion of the parasite’s life cycle in any of the 16 infected jackals certainly warrants further investigation.
The S. lupi-associated aortic pathology present in jackals is largely similar to that described in dogs, namely intimal thickening, aneurysm formation and dystrophic mineralization as a result of elastic fiber damage within the tunica media, with eventual fibrous replacement and ossification with hematopoietic tissue formation [3, 4, 15, 26]. These characteristics were also described in wild carnivores from the northern hemisphere . The most striking difference between the S. lupi-associated aortic pathology in dogs and jackals is the predominance of eosinophils within larval tracts in the jackals’ aortas. In the majority of dogs that have been necropsied in South Africa, the larval tracts consist predominantly of neutrophils and far fewer eosinophils . However, most S. lupi-induced lesions are in an advanced stage when a necropsy is requested on a dog that has died of spirocercosis, whilst dogs that have died from causes other than S. lupi might have incidental and therefore early S. lupi-induced lesions, similar to those in jackals. Thus far there has been no systematic study of early lesions in dogs. The S. lupi-induced esophageal nodule found in one jackal in this study resembled that of the early inflammatory and collagenous stage in the dog, with no worms or eggs present, no communication with the esophageal lumen and no evidence of neoplastic transformation. None of the jackals examined had caudal thoracic ventral vertebral body spondylitis, which is pathognomonic for S. lupi in dogs . In dogs, the larvae frequently show aberrant migration, for which there was no evidence in this study. Various complications following the normal and aberrant migration of larvae in the dog have been described (aortic rupture, esophageal perforation, pneumothorax, pyothorax), none of which were observed in the jackals examined.
Spirocerca-induced lesions in jackals differed from those described in wild carnivores in the northern hemisphere in that larval tracts in the jackal’s aortas were dominated by eosinophils and the jackal’s esophageal nodule was predominantly fibrous, whereas larval tracts and esophageal nodules in wild carnivores in the northern hemisphere were predominantly described as granulomatous, although in coyotes eosinophils featured prominently in the cellular infiltrate . On the other hand, Spirocerca-induced lesions in the red fox (Vulpes vulpes) have been reported as gastric and omental nodules characterized microscopically by fibroplasia and an inflammatory infiltrate consisting of lymphocytes, plasma cells, hemosiderin-laden macrophages and fewer neutrophils and eosinophils [1, 22].
Lack of communication of esophageal nodules as observed in the jackal may represent a general trend in wild carnivores. Of 150 coyotes examined in Texas (USA), only 11 (7%) had S. lupi-induced esophageal nodules and in only 5 (45%) did the worms establish communication with the esophageal lumen . In a red fox with Spirocerca-induced gastric nodules in one study, the worms did establish communication with the gastric lumen, but no S. lupi eggs were found in the feces using the fecal flotation egg count technique .
Sarcomatous transformation of the esophageal nodule and S. lupi-associated spondylitits of the ventral bodies of the caudal thoracic vertebrae were not observed in the jackals in this study and have not been reported in wild carnivores . However, aberrant larval migration has been reported in coyotes, as well as complications of larval migration in a neotropical bush dog (Speothos venaticus) and in a red fox [10, 29, 35]. Further studies are needed to establish whether aberrant larval migration or complications of larval migration occur in jackals.
The apparent low pathogenicity found in jackals in this study may suggest that spirocercosis in jackals is merely an incidental finding. However, this is purely speculative as the jackals that were culled in this study were culled for reasons unrelated to illness and the timeline and burden of infection is unknown. Furthermore, unrecorded mortalities may occur in jackals suffering from more severe infestations. Numerous theories exist to explain the differences in pathologies observed in jackals, other wild carnivores (e.g. coyotes) and domestic dogs with spirocercosis, some of which are briefly examined below.
One such theory is that jackals are much older hosts to S. lupi and have evolved resistance over time to S. lupi infection, whereas dogs might be a far more recent host [33, 43]. The predominance of eosinophils in the jackals’ and coyotes’ microscopic aortic sections may support the idea that these carnivores may have evolved resistance towards S. lupi infection. Eosinophils are potent cells capable of combatting helminth infections and maintaining tissue homeostasis, which significantly influences the efficiency of the innate immune response [6, 36] and presumably helps to minimize the S. lupi burden, thus protecting the host at the expense of the parasite .
Another theory to consider might be that the dog’s immune system is relatively immature and therefore suboptimal for dealing with S. lupi infections. During the process of selection and domestication of dogs, many of the structural modifications of modern breeds are evident in changes in the rate of development . These changes are dominated by pedomorphosis (the retention of juvenile morphological characteristics) . It is possible that pedomorphosis has also rendered the dogs’ immune system immature.
The difference in the immune response to parasitic infection between urban dogs and jackals might also be due to jackals being scavengers , as are coyotes . However, free-ranging or feral dogs are also efficient scavengers, especially in under-resourced communities . Scavengers such as jackals, coyotes, free-ranging and feral dogs have increased exposure to a wider variety and number of microorganisms and/or toxins from decomposed carcasses and refuse . Therefore, they may have evolved an improved innate immune response to infection compared to the domestic dog, which may have an inadequate innate immunity as a result of selective breeding and reduced priming of the immune system. This might explain the abundance of eosinophils in the aortic lesions of the infected jackals examined in this study. Future research should address the immune response against parasitic infections in scavenging (i.e. free-ranging and feral) dogs, versus non-scavenging (i.e. urban) dogs to further evaluate this aspect.
Finally, another aspect worthy of investigation is the composition of the intestinal microflora in jackals, free-ranging and feral dogs and urbanized domestic dogs (i.e. scavengers versus non-scavengers). Various factors such as diet, the use of antibiotics and microbial inoculation can bring about permanent or transient changes in the intestinal microflora and can involve up to 20% of the bacterial strains [25, 31]. Since the main immunological function of gut microflora is the development and maintenance of homeostasis of local and systemic immunity, the composition of the intestinal microflora should influence the immune response . Whereas it is known that antibiotics have a profound effect on the composition of intestinal microflora, the consumption of highly specialized and purified commercial diets by urban dogs is bound to influence the intestinal microflora composition versus the varied diet of jackals, coyotes and scavenger dogs . It seems feasible therefore that specialized diets and antibiotic therapy would impact on the immune response to S. lupi infection in urban dogs .