Introduction

Vector-borne nematodes are important agents of diseases in dogs and humans worldwide. Among others, these include filarial nematodes (e.g., Dirofilaria spp. and Onchocerca spp.), which are common parasites of domestic and wild animals that may eventually be transmitted to humans.

Some vector-borne nematodes are emerging, as it is the case of Onchocerca lupi in Europe and in the United States. The objective of this seminar is to provide an overview regarding dirofilariasis and onchocercosis in dogs.

Dirofilariasis

Canine dirofilariasis is a disease caused by filarial nematodes of the genus Dirofilaria, which are transmitted to dogs by mosquitoes of several genera and species. Excluding some old reports of infections by other Dirofilaria spp. in dogs, all cases of canine dirofilariasis are associated to two parasites: Dirofilaria immitis and Dirofilaria repens.

Dirofilaria immitis is a parasite of the cardiovascular system of dogs, cats and other carnivores and the causative agent of heartworm disease. While most of the D. immitis-infected dogs are asymptomatic, some dogs may develop severe life-threatening chronic disease characterized by cough, especially on exercise and early exhaustion upon exercise. In advanced cases, signs may progress to congestive heart failure. Atypical cases with aberrant nematode localization have been sporadically reported in the literature.¹

Dirofilaria repens is a parasite of the subcutaneous tissue of dogs, cats and other carnivores, being prevalent in the Old World. While the vast majority of dogs infected by D. repens are asymptomatic, some dogs may present multiple nodules in different parts of the body, including conjunctival nodules that need to be surgically removed.

Onchocercosis

Onchocerca lupi is an enigmatic parasite originally described in 1967 from a wolf in the Caucasus region of the Republic of Georgia. Now it is acknowledged that it may also infect dogs, cats and humans. Most of the infected dogs remain asymptomatic, but some dogs may present ocular lesions, including ocular nodules that are often evident on the eyelids, conjunctiva, and sclera.² Recent research indicates that O. lupi is widespread in Europe and in the United States. Recent studies have provided new insights into the diagnosis of this infection in dogs, including on the usefulness of ultrasound tools to evaluate the localization of nodules or cysts containing the adult nematode.³ Nonetheless, much has to be discovered or proven regarding this parasite, including le role of black flies (simúlidos) as vectors.⁴

Public Health Significance

Human infections by D. immitis and D. repens have been sporadically described in the literature. Human cases are usually diagnosed in areas where the infections in dogs are moderately to highly prevalent. In the Americas, D. immitis is the most common agent of human dirofilariosis⁵ and the majority of patients present a solitary, non-calcified peripheral subpleural pulmonary nodule (the so-called "coin lesion"), which is usually located in the lower lobes and is detected during routine X-ray examinations. While most human patients do not show apparent clinical signs, some individuals may present cough, chest pain, haemoptysis, and dyspnoea.⁵ A recent case of ocular infection by a Dirofilaria sp. close to D. immitis raised interesting questions regarding the genetic variability of this species.⁶

After the first evidence of human infection by O. lupi in Turkey,⁷ new human cases have been described in Tunisia, Germany, Hungary, Greece, Portugal, Iran and the United States⁸. Human patients usually present painless subconjunctival nodules that need to be surgically removed. Interestingly, American patients have not had subconjunctival nodules but spinal, orbital, and subdermal nodules.⁹

Conclusions

Dirofilariasis and onchocercosis are neglected zoonoses that should be included in the list of differential diagnosis of both veterinary practitioners and medical physicians working in endemic areas. New tools have been developed for the diagnosis of both diseases in dogs and humans.^3,10

From a One Health viewpoint, veterinary practitioners, medical physicians, and public health authorities should work together towards the prevention of these diseases. For dirofilariasis, it is crucial to educate dog owners regarding the use of preventive measures (e.g., repellents and monthly administration of macrocyclic lactones). For onchocercosis, further studies are needed to prove the vector role of black flies, as this information would pave the way for the elaboration of preventive measures to reduce the risk of infection in both dogs and humans.

References

1.  Dantas-Torres F, Lia RP, Barbuto M, Casiraghi M, Crovace A, Caligiani L, Genchi C, Otranto D. Ocular dirofilariosis by Dirofilaria immitis in a dog: first case report from Europe. J Small Anim Pract. 2009;50(12):667–9.

2.  Otranto D, Giannelli A, Scotty Trumble N, Chavkin M, Kennard G, Latrofa MS, Bowman DD, Dantas-Torres F, Eberhard ML. Clinical case presentation and a review of the literature of canine onchocercosis by Onchocerca lupi in the United States. Parasit Vectors. 2015;8:89.

3.  Franchini D, Giannelli A, Di Paola G, Cortes H, Cardoso L, Lia RP, Campbell BE, Dantas-Torres F, Lenoci D, Assad EA, Ricciardi M, Valastro C, Cavaliere L, Di Bello A, Otranto D. Image diagnosis of zoonotic onchocercosis by Onchocerca lupi. Vet Parasitol. 2014;203(1–2):91–5.

4.  Hassan HK, Bolcen S, Kubofcik J, Nutman TB, Eberhard ML, Middleton K, Wekesa JW, Ruedas G, Nelson KJ, Dubielzig R, De Lombaert M, Silverman B, Schorling JJ, Adler PH, Unnasch TR, Beeler ES. Isolation of Onchocerca lupi in dogs and black flies, California, USA. Emerg Infect Dis. 2015;21(5):789–96.

5.  Dantas-Torres F, Otranto D. Dirofilariosis in the Americas: a more virulent Dirofilaria immitis? Parasit Vectors. 2013;6(1):288.

6.  Otranto D, Diniz DG, Dantas-Torres F, Casiraghi M, de Almeida IN, de Almeida LN, dos Santos JN, Furtado AP, de Almeida Sobrinho EF, Bain O. Human intraocular filariasis caused by Dirofilaria sp. nematode, Brazil. Emerg Infect Dis. 2011;17(5):863–6.

7.  Otranto D, Sakru N, Testini G, Gürlü VP, Yakar K, Lia RP, Dantas-Torres F, Bain O. Case report: first evidence of human zoonotic infection by Onchocerca lupi (Spirurida, Onchocercidae). Am J Trop Med Hyg. 2011;84(1):55–8.

8.  Grácio AJ, Richter J, Komnenou AT, Grácio MA. Onchocerciasis caused by Onchocerca lupi: an emerging zoonotic infection. Systematic review. Parasitol Res. 2015;114(7):2401–13.

9.  Cantey PT, Weeks J, Edwards M, Rao S, Ostovar GA, Dehority W, Alzona M, Swoboda S, Christiaens B, Ballan W, Hartley J, Terranella A, Weatherhead J, Dunn JJ, Marx DP, Hicks MJ, Rauch RA, Smith C, Dishop MK, Handler MH, Dudley RW, Chundu K, Hobohm D, Feiz-Erfan I, Hakes J, Berry RS, Stepensaski S, Greenfield B, Shroeder L, Bishop H, de Almeida M, Mathison B, Eberhard M. The emergence of zoonotic Onchocerca lupi infection in the United States - A case-series. Clin Infect Dis. 2016;62(6):778–83.

10. Latrofa MS, Dantas-Torres F, Annoscia G, Genchi M, Traversa D, Otranto A duplex real-time polymerase chain reaction assay for the detection of and differentiation between Dirofilaria immitis and Dirofilaria repens in dogs and mosquitoes. Vet Parasitol. 2012;185(2–4):181–5.