Nicole Szafranski
DVM
Dr. Szafranski is a graduate of the University of Tennessee College of Veterinary Medicine (UTCVM) and is the current Zoetis veterinary parasitology resident at UTCVM through the National Center for Veterinary Parasitology. She is pursuing a PhD through the University of Tennessee’s College of Comparative and Experimental Medicine, focusing on Toxoplasma gondii in waterfowl. Her research interests include zoonotic parasites and the diagnosis and management of parasitic diseases in wildlife and domestic animals.
Read Articles Written by Nicole SzafranskiRichard Gerhold
DVM, MS, PhD, DACVM (Parasitology)
Dr. Gerhold received his BS in wildlife science and DVM from Purdue University. He received his MS and PhD from the University of Georgia for investigating various parasites of wild and domestic mammals and birds. He is also a board-certified parasitologist. He is currently an associate professor of parasitology at the College of Veterinary Medicine at University of Tennessee. His research interests include parasites associated with wildlife and public health; avian diseases; and vector-borne diseases.
Read Articles Written by Richard Gerhold
With many dogs being kept to a primarily indoor lifestyle, trematode or “fluke” infections of companion animals have decreased in notoriety in recent years. Trematodes are more often thought of as agents of cattle or small ruminant infections or human tropical diseases than as parasites of dogs and cats.1,2 However, many trematodes still warrant consideration as canine parasites in the United States.
The epidemiology and pathophysiology of the flukes that infect dogs are varied and complex; however, flukes are generally categorized based on the primary organ they infect. The major categories of flukes are respiratory (lung), intestinal, hepatopancreatic, and vascular (blood). Fluke-infected dogs can present with a range of clinical signs that often overlap with those of many other diseases, such as lethargy, hyporexia, vomiting, and diarrhea. A patient’s clinical and geographic history are helpful indicators of when a fluke infection should be more strongly considered as a potential diagnostic differential.
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Lung Flukes
The main lung flukes that infect dogs are from the genus Paragonimus, with Paragonimus kellicotti and Paragonimus westermani being most notable. While P westermani is worth mentioning as it is of canine and zoonotic concern, it is not currently found in the United States.
Life Cycle
P kellicotti can be found throughout much of the eastern United States, and the adult flukes (7.5 to 12 mm × 4 to 6 mm) are found in cysts in the lungs of a variety of wild and domestic mammals, including dogs and cats. This fluke uses 2 intermediate hosts to complete its life cycle. The first intermediate host is a snail of the Pomatiopsis genus, and the second is either a crayfish (Cambarus species, Orconectes species) or a freshwater crab.2,3 A dog becomes infected by ingesting a crab or crayfish infected with metacercariae. The metacercariae excyst in the lumen of the dog’s duodenum, penetrate the intestinal wall, and make their way into the peritoneal cavity, through the diaphragm, and into the lungs. Once in the lungs, they encyst, develop into adult flukes, reproduce, and release eggs which are eventually coughed up, swallowed, and passed in the dog’s feces.
Diagnosis
While not common, P kellicotti infection should not be forgotten when a dog presents with respiratory signs. The clinical presentation of a P kellicotti infection can range from severe respiratory distress due to a pneumothorax to nondescript respiratory signs (e.g., coughing, dyspnea) to entirely asymptomatic.4 Consider this fluke in cases in which infectious pneumonias of other causes (e.g., bacterial, viral, fungal), intrathoracic neoplasia, and spontaneous pneumothorax due to a bulla rupture have been ruled out. Diagnosis is often made from identifying the characteristic eggs, which are 80 to 100 µm × 55 to 65 µm in size, are brown in color, and have a distinct operculum on one end. Most trematode eggs are relatively heavy and do not float well in many flotation solutions. However, Paragonimus eggs are an exception and can often be found using a sugar-based solution. In addition, centrifugation is strongly recommended to increase the sensitivity of fecal flotation as a diagnostic tool for this parasite and other flukes.5 The pulmonary cysts may also be visible on radiographs as poorly marginated soft tissue opacities in early infections or as air-filled pneumocysts due to cyst rupture in more chronically infected patients with the potential for pneumothorax development.6
Treatment
No parasiticide is specifically labeled for treatment of Paragonimus infections in dogs; however, successful treatment is often achieved using praziquantel (23 mg/kg q8h PO for 3 days), albendazole (25 mg/kg q12 for 10 days), or fenbendazole (50 mg/kg q24h PO for 10 to 14 days).1
Intestinal Flukes
The intestinal trematode that garners the most attention in the United States, particularly in the northwestern states, is Nanophyetus salmincola, which is a carrier of the bacterium Neorickettsia helminthoeca; this infection is also called “salmon poisoning.” However, other gastrointestinal (GI) flukes deserve acknowledgment, including Alaria species (i.e., Alaria americana/canis, Alaria marcianae, and Alaria arisemoides), Apophallus venustus, and Cryptocotyle lingua. These flukes can present with signs akin to those of GI diseases such as pancreatitis, acute hemorrhagic diarrhea syndrome (AHDS; previously hemorrhagic gastroenteritis), neoplasia, fungal diseases (e.g., Coccidioides immitis in western states), and bacterial or viral enteritis.
Nanophyetus salmincola
Life Cycle
Adults of N salmincola live attached to the mucosa of the small intestine in their definitive hosts. These flukes have a complex 3-host life cycle, during which they spend time developing in freshwater snails (i.e., Oxytrema silicula), salmonid fish (e.g., salmon, trout), and carnivorous mammals (e.g., dog, cat, bear, fox, raccoon). Dogs become infected by ingesting raw or undercooked fish containing the fluke metacercariae, and while the fluke itself does not cause much harm, the bacteria it can carry are quite virulent.
Clinical Signs
N helminthoeca is a gram-negative rickettsia that can cause severe disease in dogs.7,8 Clinical signs develop within 1 to 4 weeks after infection and include high fever, anorexia, lethargy, hemorrhagic diarrhea, and generalized lymphadenopathy. Geographic location (i.e., Pacific Northwest) and patient history (e.g., history of eating raw/undercooked fish, spending time outdoors at natural water sources), along with N salmincola egg identification on fecal flotation, play into the diagnosis. The eggs range in size from 35 to 55 µm × 72 to 97 µm, appear oval to pear-shaped, and are passed unembryonated in the dog’s feces.2,9 Diagnosis of the bacterial infection can be confirmed via polymerase chain reaction (PCR) performed at a referral diagnostic laboratory.
Treatment
Treatment includes treating the fluke infection with praziquantel (10 to 30 mg/kg, one dose PO or SC) and the bacterial infection with doxycycline (5 to 10 mg/kg q12h PO or IV for 21 days) or tetracycline (22 mg/kg q8h PO for 21 days). Without proper treatment, N helminthoeca can have a mortality rate of up to 90% in dogs.
Alaria Species
Life Cycle
Alaria flukes use 3 different hosts to complete their life cycle: freshwater snails (first intermediate host); tadpoles (second intermediate host); and carnivores, such as dogs, cats, and foxes (definitive host). Dogs become infected by ingesting either an infected tadpole or an infected paratenic host (e.g., frog, snake, rodent).1,10 Puppies may become infected through lactogenic transmission.
Adult flukes are found in the dog’s small intestine and generally do not cause much harm, although GI signs may be seen with a heavy fluke burden. The immature flukes migrate through the lungs before reaching the small intestine to mature and may cause some respiratory signs due to trauma. The diagnosis of Alaria infections is sporadic around the country, occurring primarily in temperate regions, and most cases are associated with dogs that prey on small mammals, amphibians, or reptiles.11,12
Diagnosis and Treatment
Fecal flotation and patient history aid in diagnosis.13 On fecal sedimentation and/or flotation, Alaria eggs are 108 to 110 µm × 64 to 76 µm in size, unembryonated, oval, and delicately operculated. Praziquantel is the most common treatment and is often successful; however, no medications are approved for the treatment of Alaria infections. Care should be taken to educate owners on the importance of discouraging their dogs from eating frogs, snakes, and rodents. It is best to not leave dogs unattended in the yard or allow them off leash without careful supervision.
Other Species
A venustus and C lingua infections are uncommon in dogs but have been reported historically.14 A venustus infects freshwater fish, whereas C lingua infects marine fish; birds and mammals (including dogs) become infected by ingesting infected fish.15 Diagnosis is achieved by fecal sedimentation and/or flotation, geographic location, and patient history. Eggs of both species are quite heavy and can be missed using passive fecal flotation techniques when centrifugation is not utilized. There are no approved drugs for the treatment of either fluke. Treatment with praziquantel has been suggested but remains unproven.3
Hepatopancreatic Flukes
In the United States, the fluke species that cause infections of the liver, bile ducts, and pancreas are very rarely found in dogs, but a few are worth briefly noting: Metorchis conjunctus (primarily seen in foxes and swine);12 the raccoon pancreatic fluke, Eurytrema procyonis (more often reported in cats); and Clonorchis sinensis and Opisthorchis tenuicollis (syn. Opisthorchis felineus), which can infect dogs, cats, and humans and may rarely be found in dogs originally from regions in Eurasia.16-19
While rare, these flukes should be considered in canine patients when pancreatitis, cholangitis and/or cholecystitis, and hepatitis have been ruled out. In dogs with compromised exocrine pancreatic tissue (e.g., chronic pancreatitis), heavy infections with E procyonis can further damage the pancreatic parenchyma, leading to clinical signs of exocrine pancreatic insufficiency.20 Eggs passed in the dog’s feces are roughly 20 to 30 µm in size, except for E procyonis, which has eggs measuring 45 to 53 µm × 29 to 36 µm.20 There are no approved treatments for these parasites in dogs in the United States, but typical praziquantel administration will likely be successful.21
Blood Flukes
The blood fluke (schistosome) of concern in U.S. dogs is Heterobilharzia americana. This fluke can be colloquially referred to as “swimmer’s itch” or “swamp itch,” although avian schistosomes are more often implicated in causing this pruritic dermatitis in humans. In dogs, the skin lesions are not the primary concern; however, they may be confused with a bacterial or allergic dermatitis.
H americana is found throughout the Gulf Coast region and other coastal southeastern states. Its range is currently expanding, with cases being noted in Oklahoma, Kansas, and Texas in the past decade.22 It uses aquatic lymnaeid snails as its intermediate hosts and typically raccoons as its definitive hosts; however, dogs, nutria, and bobcats can also act as final hosts.2
Life Cycle
The motile stage that emerges from the snail into the water (i.e., cercaria) penetrates the skin and vasculature of the dog, making its way through the lungs and liver before reaching the mesenteric veins to mature. Eggs are released by the females and penetrate the intestinal wall to be passed in the feces. The accumulation of eggs can lead to severe granulomatous inflammation of the liver and GI tract, causing signs such as diarrhea, vomiting, polyuria, polydipsia, and weight loss. Other differentials to rule out include GI and hepatic neoplasia, endocrine disorders (e.g., Cushing’s disease/hyperadrenocorticism), and AHDS.
With such a varied list of potential clinical signs and diagnostic differentials, the lifestyle and travel history of the patient are important in guiding the placement of blood flukes higher or lower on the differential list. A middle-aged dog from the Midwest that only goes outside for leashed walks is far less likely to be infected than a young hunting dog from a Gulf Coast state that spends most of its time outside exploring wetlands. Discussing patient history with the owner can be an invaluable asset in making a blood fluke diagnosis.
Diagnosis
Diagnosis is often multifaceted, including fecal sedimentation or flotation in a saline solution, serum chemistry and complete blood count, abdominal ultrasonography, and molecular diagnostics. Great strides have been made in various molecular techniques, including PCR and antigen-capture ELISA (enzyme-linked immunosorbent assay) testing. On fecal examination, H americana eggs lack an operculum, appear thin-shelled, and are 70 to 90 µm in size. Serum chemistry abnormalities often include hypercalcemia and elevated liver enzymes.
Treatment
Treatment success is variable, with earlier diagnosis leading to better outcomes. Current recommendations include combination treatment with praziquantel (10 mg/kg q8h PO for 2 days) and fenbendazole (24 mg/kg q24h PO for 7 days).23
Clinical Applications
Trematodes have complex life cycles with unique intermediate hosts, and infections come with varied clinical signs and geographic distributions. With many dogs living most of their lives indoors, the presumed incidence of fluke infections has declined over the decades, but trematodes should not be forgotten entirely in everyday practice. Patient history can offer a clue as to when trematodiasis should shift higher up the differential list. Risk factors such as geographic regional differences, lifestyle habits, dietary choices, and pet travel should also be investigated, as they can offer significant insight into when to look for a trematode infection, and which one. The next time a dog comes in with vague respiratory or GI signs, consider whether it could be “just” a fluke.
References
1. Helminths. In: Bowman DD. Georgi’s Parasitology for Veterinarians. 11th ed. Elsevier; 2021:135-262.
2. Georgi JR, Georgi ME. Trematodes. In: Cann C, ed. Canine Clinical Parasitology. Lea & Febiger; 1991:101-122.
3. Chai JY. Epidemiology of trematode infections. In: Toledo, R, Fried B, eds. Digenetic Trematodes. 2nd ed. Springer; 2019:359-410.
4. Fischer PU, Curtis KC, Marcos LA, Weil GJ. Molecular characterization of the North American lung fluke Paragonimus kellicotti in Missouri and its development in Mongolian gerbils. Am J Trop Med Hyg. 2011;84(6):1005-1011.
5. Nagamori Y, Payton ME, Looper E, et al. Retrospective survey of endoparasitism identified in feces of client-owned dogs in North America from 2007 through 2018. Vet Parasitol. 2020;282:1-9.
6. Broman MM, Miller MA. Pathology in practice. JAVMA. 2016;248(11):1253-1255.
7. Greiman SE, Kent ML, Betts J, et al. Nanophyetus salmincola, vector of the salmon poisoning disease agent Neorickettsia helminthoeca, harbors a second pathogenic Neorickettsia species. Vet Parasitol. 2016;229:107-109.
8. Headley SA, Scorpio DG, Vidotto O, Dumler JS. Neorickettsia helminthoeca and salmon poisoning disease: a review. Vet J. 2011;187(2):165-173.
9. Diagnostic parasitology. In: Bowman DD. Georgi’s Parasitology for Veterinarians. 11th ed. Elsevier; 2021:349-454.
10. Dyer NW, Greve JH, Bartholomay B. Alaria arisaemoides in a black Labrador retriever pup. J Vet Diagn Invest. 1997;9(2):203-205.
11. Gaunt MC, Carr AP. A survey of intestinal parasites in dogs from Saskatoon, Saskatchewan. Can Vet J. 2011;52(5):497-500.
12. Sitko J, Bizos J, Sherrard-Smith E, et al. Integrative taxonomy of European parasitic flatworms of the genus Metorchis Looss, 1899 (Trematoda: Opisthorchiidae). Parasitol Int. 2016;65(3):258-267.
13. Riehn K, Hamedy A, Alter T, Lucker E. Development of a PCR approach for differentiation of Alaria spp. mesocercariae. Parasitol Res. 2011;108(5):1327-1332.
14. Wapenaar W, Barkema HW, O’Handley R. Fecal shedding of Toxocara canis and other parasites in foxes and coyotes on Prince Edward Island, Canada. J Wildl Dis. 2013;49(2):394-397.
15. Byers JE. Effects of climate change on parasites and disease in estuarine and nearshore environments. PLoS Biol. 2020;18(11):e3000743.
16. Doanh PN, Nawa Y. Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects. Trans R Soc Trop Med Hyg. 2016;110(1):13-20.
17. Gabrielli AF. Dogs and trematode zoonoses. In: Macpherson CNL, Meslin FX, Wandeler AI, eds. Dogs, Zoonoses, and Public Health. 2nd ed. CABI; 2013:109-126.
18. Ye CY, Yang ZD, Zheng HL. Fatal multi-organ Clonorchis sinensis infection in dog: a case report. Vet Parasitol. 2013;195(1-2):173-176.
19. Capen CC. Endocrine system. In: Thomson’s Special Veterinary Pathology. 3rd ed. Mosby; 2001:279-323.
20. Carney WP, Schilling PW, McKee AE, et al. Eurytrema procyonis, a pancreatic fluke of North American carnivores. J Wildl Dis. 1970;6(4):422-429.
21. Lemetayer JD, Snead EC, Starrak GS, Wagner BA. Multiple liver abscesses in a dog secondary to the liver fluke Metorchis conjunctus treated by percutaneous transhepatic drainage and alcoholization. Can Vet J. 2016;57(6):605-609.
22. Rodriguez JY, Lewis BC, Snowden KF. Distribution and characterization of Heterobilharzia americana in dogs in Texas. Vet Parasitol. 2014;203(1-2):35-42.
23. Graham AM, Davenport A, Moshnikova VS, et al. Heterobilharzia americana infection in dogs: a retrospective study of 60 cases (2010-2019). J Vet Intern Med. 2021;35(3):1361-1367.