Canine Pulmonary Helminths: Recommendations from the Companion Animal Parasite Council

Dwight D. Bowman, MS, PhD, Diplomate ACVM (Parasitology, Hon),
Cornell University

Susan E. Little, DVM, PhD, Diplomate ACVM (Parasitology),
Oklahoma State University

Pulmonary helminths can cause severe, life-threatening respiratory disease in dogs. Distribution, life cycle, diagnosis, and treatment of common species are discussed.

Helminth parasites are regularly diagnosed in dogs in the U.S. Those in dogs typically fall into 1 of 2 categories: intestinal helminths or pulmonary helminths. Canine intestinal helminths were discussed in this column in the January/February 2014 issue, available at tvpjournal.com; this article will address canine pulmonary helminths. 

PULMONARY HELMINTHS

A surprisingly wide variety of helminths damage the pulmonary system of dogs and, at times, can cause severe, life-threatening respiratory disease (Table 1). 

• Dirofilaria immitis (heartworm) is by far the most important parasite of the canine pulmonary system, inducing severe morbidity and, in some cases, mortality.
• Toxocara canis and Ancylostoma caninum are intestinal nematodes that migrate through the lungs as larvae. 
• Paragonimus kellicotti is a trematode that develops in cysts in the lung parenchyma.¹
• Angiostrongylus vasorum, the French heartworm, and the lungworms Crenosoma vulpis, Eucoleus aerophilus, and Filaroides species also create pathology in canine lungs.

While less familiar than heartworm, infection with these other pulmonary helminths can be very important in some canine patients. This article outlines how dogs become infected and describes appropriate treatment courses to manage the infections.

Angiostrongylus vasorum

Distribution. Once considered exotic to North America, A vasorum, commonly known as the French heartworm, has in recent years been found in foxes and dogs in the Atlantic provinces of Canada as well as in the U.S.²

Life Cycle. Dogs acquire infection when they eat infected gastropod intermediate hosts (snails or slugs) or frog paratenic hosts. Upon ingestion, larvae first develop in abdominal lymph nodes before entering the portal circulation and moving to the pulmonary arteries and right ventricle. Once in the lungs, the nematodes mature to adults (Figure 1), mate, and produce eggs that lodge and develop in pulmonary capillaries. Larvae that hatch from the eggs move into an airspace; then are coughed up, swallowed, and passed in the feces. Snails and slugs feeding on the feces ingest the larvae and perpetuate the life cycle.³

Figure 1. Three adult female Angiostrongylus vasorum, showing the “barber pole” appearance caused by the reproductive tract wrapping around the intestinal tract of the worm.

Clinical Signs. Infection with A vasorum produces disease similar to that caused by D immitis: chronic cough, dyspnea, exercise intolerance, and anorexia. 

• Gagging and weight loss are the most common clinical signs reported. 
• Pulmonary hemorrhage can occur as larvae migrate into airspaces. 
• Granulomas develop in response to eggs and larvae, and pulmonary fibrosis occurs.
• Pulmonary vascular lesions include thromboarteritis and intimal proliferation; pulmonary hypertension can lead to congestive right heart failure.⁴

Diagnosis. Larvae can be detected in feces using the Baermann technique or fecal flotation, and are identified by the characteristic kink at the tip of the tail (Figure 2). Radiographic changes associated with A vasorum infection include:

• Diffuse peribronchial, interstitial, and alveolar densities
• Enlargement of the right heart and pulmonary artery.

Figure 2. Posterior end of tail of first-stage Angiostrongylus vasorum larva in feces, demonstrating the tail kink just posterior to the tip.

Treatment (Table 2). Infections have been treated with several different types of anthelmintics:

• Albendazole or fenbendazole
• Ivermectin 
• Levamisole
• Moxidectin.

Severe dyspnea and ascites may be seen after treatment; bronchodilators, expectorants, and diuretics may be required to manage these post-treatment reactions.

Prevention. Routine administration of topical moxidectin has been shown to protect dogs from infection with this parasite.⁵ Dogs can also be protected by minimizing opportunities to consume snails, slugs, and frogs.

Crenosoma vulpis

Distribution. This lungworm of foxes and other wild canidae is most common in the northeastern U.S. and the eastern part of Canada.⁶

Life Cycle. Dogs become infected when, like foxes, they ingest the snail or slug intermediate host. The nematodes migrate to the lungs and develop into adults, moving from the smaller bronchioles to the larger bronchi as they mature.

Clinical Signs. Infections may be asymptomatic or can induce bronchitis and bronchiolitis, resulting in chronic cough.⁷

Diagnosis. Infection with C vulpis is confirmed by identifying characteristic larvae with a conical head and conical, tapering tail (Figure 3) in the feces, or finding the worms in the bronchi at necropsy.

Figure 3. Posterior end of tail of first-stage Crenosoma vulpis larva in feces, demonstrating the conical, tapering tail.

Treatment (Table 2). Successful treatments described in the literature include fenbendazole, ivermectin, and febantel. More recently, excellent results have been obtained using:

• Milbemycin oxime at 0.5 mg/kg PO single dose 
• Topical application of 10% moxidectin, single dose.^8,9

Prevention. Routine use of monthly parasite control products containing milbemycin oxime or moxidectin are expected to prevent establishment of future infections.

Eucoleus aerophilus

Distribution. Infection with E aerophilus is seen wherever dogs and cats are found, although foxes are considered an important reservoir host.¹⁰

Life Cycle. Eggs are shed in the sputum or feces, and embryonate in 30 to 50 days. Larvae are released when eggs or earthworm paratenic hosts are ingested and migrate by the bloodstream to the lungs. The larvae then penetrate the alveoli and migrate up the air passages as they develop. They reach maturity in the epithelium of the bronchioles, bronchi, and trachea, threading their thin bodies through the epithelial surface.¹

Clinical Signs. Most infections with E aerophilus are clinically inapparent. If large numbers of nematodes are present, dogs may develop tracheitis, bronchitis and, sometimes, pneumonia,¹¹ which can cause: 

• Anorexia
• Cough
• Debilitation
• Dyspnea
• Nasal discharge. 

Diagnosis. The eggs passed in sputum or feces are characteristic, with polar plugs that are slightly askew of the central axis (Figure 4) and a granular shell. The eggs in the feces of dogs must be differentiated from those of Trichuris vulpis (larger), Eucoleus boehmi (contain a partially developed embryo when passed), and Pearsonema plica (present in feces contaminated with urine).¹

Treatment (Table 2) & Prevention. Extended courses of ivermectin or fenbendazole have been reportedly successful at eliminating infection, but anecdotal evidence suggests that routine preventives may not be protective against this nematode.

Figure 4. Egg of Eucoleus aerophilus in feces, with typical polar plugs that are slightly askew of vertical between each end.

Filaroides species

Distribution. Infection with Filaroides species occurs sporadically, and periodically appears in some kennels or in individual dogs.¹²

Life Cycle. Larvae shed in the feces or in the respiratory secretions of infected dogs are immediately infective and may be transmitted to other dogs by ingestion; this direct life cycle facilitates rapid spread between co-housed dogs. Ingested larvae migrate to the trachea and develop into adults in nodules (F osleri) or the lung parenchyma (F hirthi).

Clinical Signs. Infection with F osleri can cause a hard, dry cough triggered by exercise or exposure to cold air.¹² Young dogs are most acutely affected and sometimes develop respiratory distress, anorexia, and emaciation.

Infection with F hirthi is usually asymptomatic, but fatal cases of hyperinfection have developed in severely stressed and immunodeficient animals.¹³

Diagnosis. Infection with Filaroides species is diagnosed by finding larva with fecal flotation using zinc-sulfate centrifugation. Larva of: ¹⁴

• F osleri have a constriction and a kink just posterior to the end of the tail (Figure 5).
• F hirthi come to a simple point at the tip of the tail (Figure 6).

Infection with F osleri may also be diagnosed at bronchoscopy by identifying the pathognomonic transparent submucosal nodules containing nematodes.

Figure 5. Posterior end of tail of first-stage Filaroides osleri larva in feces, demonstrating the dorsal kink just terminal to the end of the tail.

Figure 6. Posterior end of tail of first-stage Filaroides hirthi larva in feces, demonstrating the tapering conical tail.

Treatment (Table 2). The treatment of choice for F osleri seems to be injectable doramectin; some veterinarians also remove as many nodules as possible with the aid of the bronchoscope. Dogs with both F osleri and F hirthi have also been successfully treated with several days of fenbendazole or ivermectin.

Prevention. Because larvae of Filaroides species are immediately infective when shed in the feces, control can be difficult, particularly if other canine members of the household are infected.¹⁵

Paragonimus kellicotti

Distribution. Infection with P kellicotti occurs along the Mississippi, Missouri, Ohio, and St. Lawrence rivers and in areas of the southeastern U.S.¹⁶

Life Cycle. Eggs passed in the feces hatch to release a miracidium, which penetrates a snail. Cercariae are produced that leave the snail host and enter a crayfish to encyst as metacercariae. When the crayfish is eaten by a dog, cat, other wild carnivore, or a human, adult trematodes develop within cysts in the lung parenchyma. Paratenic hosts that ingest infected crayfish may also harbor infective metacercariae.¹

Clinical Signs. Dogs infected with P kellicotti may be asymptomatic or can present with a variety of respiratory signs, including:

• Coughing
• Dyspnea
• Bronchiectasis
• Hemoptysis.

Dogs may tolerate a low number of intact cysts, but in heavy infections, or when cysts rupture, severe disease may result due to:¹⁷

• Pulmonary hemorrhage
• Pneumothorax
• Granulomatous pneumonia.

Diagnosis. Eggs of P kellicotti can be recovered by sugar flotation, sedimentation of feces, or transtracheal wash, and are characterized by their size, seated operculum, and abopercular bump or flange on the end opposite the operculum (Figure 7). Pulmonary cysts may be evident on thoracic radiographs.

Figure 7. Paragonimus kellicotti egg in feces collected via sedimentation, demonstrating the seated operculum and the abopercular flange or bump.

Treatment (Table 2). Infections may be treated with repeated courses of any of the following:¹⁸

• Albendazole
• Fenbendazole
• Praziquantel.

RISK FOR ZOONOTIC INFECTION

Several of the common canine pulmonary helminths are zoonotic, although infections are acquired from the environment or a vector, rather than direct contact with infected dogs. 

• Toxocariasis upon ingestion of infective eggs of T canis from contaminated soil is well documented; as many as 1 in 7 adults in the U.S. harbor antibodies to Toxocara species.¹⁹
• Human infection with D immitis via mosquitoes also occurs, resulting in development of pulmonary granulomata.²⁰
• Human infection with P kellicotti following ingestion of raw crayfish has also been reported in young men and is associated with alcohol consumption.¹⁶

Protecting dogs from infection with pulmonary helminths limits environmental contamination, reducing risk of both canine and human disease.

GENERAL CONSIDERATIONS & CAPC RECOMMENDATIONS

• Administer broad-spectrum parasite control products that provide internal parasite control and prevent heartworm infection to all pet dogs year-round.
• Routinely deworm puppies beginning at 2 weeks of age, with deworming repeated every 2 weeks.
• Begin administering a monthly control product with efficacy against intestinal helminths when puppies reach 4 to 8 weeks of age. 

Other preventive measures that owners can implement include:

• Keeping dogs on a leash or in a fenced yard to prevent predation and scavenging activities; this limits the opportunity for dogs to acquire infection via ingestion of vertebrate hosts (ascarids) or from a feces-contaminated environment 
• Promptly removing feces from the yard to prevent eggs from decomposing with fecal material or dispersing into the environment.

References

1. Bowman DD. Georgis’ Parasitology for Veterinarians, 10th ed. St. Louis: Elsevier Saunders, 2014, pp 477.
2. Kistler WM, Brown JD, Allison AB, et al. First report of Angiostrongylus vasorum and Hepatozoon from a red fox (Vulpes vulpes) from West Virginia, U.S.A. Vet Parasitol 2013; 200:216-220.
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6. Conboy G. Natural infections of Crenosoma vulpis and Angiostrongylus vasorum in dogs in Atlantic Canada and their treatment with milbemycin oxime. Vet Rec 2004; 155:16-18.
7. Unterer S, Deplazes P, Arnold P, et al. Spontaneous Crenosoma vulpis infection in 10 dogs: Laboratory, radiographic and endoscopic findings. Schweiz Arch Tierheilkd 2002; 144(4):174-179. 
8. Conboy G, Hare J, Charles S, et al. Efficacy of a single topical application of Advantage Multi (=Advocate) topical solution (10% imidocloprid + 2.5% moxidectin) in the treatment of dogs experimentally infected with Crenosoma vulpis. Parasitol Res 2009; 105(S1):S49-S54.
9. Conboy G, Bourque A, Miller L, et al. Efficacy of Milbemax (milbemycin oxime + praziquantel) in the treatment of dogs experimentally infected with Crenosoma vulpis. Vet Parasitol 2013; 198:319-324.
10. Traversa D, Di Cesare A, Milillo P, et al. Infection by Eucoleus aerophilus in dogs and cats: Is another extra-intestinal parasitic nematode of pets emerging in Italy? Res Vet Sci 2009; 87(2):270-272.
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15. Georgi JR, Georgi ME, Fahnestock GR, Theodorides VJ. Transmission and control of Filaroides hirthi lungworm infection in dogs. Am J Vet Res 1979; 40(6):829-831.
16. Lane MA, Marcos LA, Onen NF, et al. Paragonimus kellicotti fluke infections in Missouri, USA. Emerg Infect Dis 2012; 18(8):1263-1267.
17. Harrus S, Nyska A, Colorni A, Markovics A. Sudden death due to Paragonimus kellicotti infection in a dog. Vet Parasitol 1997; 71(1):59-63.
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20. Theis JH. Public health aspects of dirofilariasis in the United States. Vet Parasitol 2005; 133:157-180.

Dwight D. Bowman, MS, PhD, Diplomate ACVM (Parasitology, Hon) is professor of parasitology at Cornell University College of Veterinary Medicine. He received his MS and PhD in parasitology from Tulane University.

Susan E. Little, DVM, PhD, Diplomate ACVM (Parasitology), is the director of the National Center for Veterinary Parasitology at Oklahoma State University’s Center for Veterinary Health Sciences. She received her DVM from Virginia Tech.