Persistent and disseminated infections with Strongyloides Stercoralis in immunosuppressed dogs
Abstract
The effects of immunosuppression on the course of infection in dogs infected with a human strain of S. stercoralis were investigated. Four dogs were infected then 4 weeks later, three animals were begun on prednisolone orally in a dose of 150 mg daily for 6 days each week. Rhabditiform larvae continued to be excreted in the stools. After 5 weeks of immunosuppression, one dog was autopsied; plentiful parasites were found in the upper small bowel but worms were not seen in other tissues. Similar findings were made in a second dog killed after 9 weeks of immunosuppression. In the third dog, the dose of prednisolone was increased to 225 mg daily 15 weeks after infection then azathioprine 100 mg daily was added 6 weeks later. This animal was killed 24 weeks after infection and evidence for multiplication of S. stercoralis was obtained. Large numbers of adult worms, eggs and rhabditiform larvae were recovered from duodenal fluid. Infective larvae were seen in homogenised lung, rhabditiform larvae were noted in homogenised spleen and both rhabditiform larvae and adult worms were found in homogenised kidney. Worms in all stages of development were seen in the urine. Histological examination revealed large numbers of adult worms and enormous numbers of eggs and larvae in the duodenal mucosa. Worms were seen throughout the length of the small intestine as well as in the colonic mucosa. The lungs displayed focal haemorrhages and larvae were seen in the alveolar spaces, bronchioles and bronchi. Evidence of immunosuppression was provided by the gross atrophy of the thymus and the fall in anti-Strongyloides antibody titres. In contrast to these dogs, larvae disappeared from the non-immunosuppressed dog by 13 weeks after infection. This animal was then immunosuppressed for 8 weeks but parasites could not be found in either the stools or at autopsy. Two further dogs were immunosuppressed before infection but they died soon thereafter. It is concluded that immunosuppression permits the persistence of infection with S. stercoralis and if continued for long enough and in sufficient degree, that disseminated infection supervenes. This model may provide a means for assessing the efficacy of various therapeutic regimens in overwhelming strongyloidiasis and for investigations of the host-parasite relationship in this infection.
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Cited by (39)
Miscellaneous Nematode Infections
2022, Greene's Infectious Diseases of the Dog and Cat, Fifth EditionPhysaloptera spp. Infection
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Cause: Physaloptera praeputialis and Physaloptera rara.
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First Described: Physaloptera praeputialis was first isolated from a domestic cat and described in 1889 (von Linstow). Physaloptera rara was first isolated from a domestic dog in North America and described in 1918 (Hall and Wigdor).
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Affected Hosts: Domestic and wild dogs and cats.
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Geographic Distribution: Worldwide (P. praeputialis), North America (P. rara).
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Route of Transmission: Ingestion of intermediate insect or paratenic hosts.
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Major Clinical Signs: May cause chronic intermittent vomiting. Infections often are subclinical.
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Differential Diagnosis: Any GI or systemic cause of chronic vomiting (e.g., idiopathic gastritis, gastric foreign body, gastric neoplasia, food intolerance/allergy, chronic pancreatitis). Eggs must be differentiated from those of Spirocerca lupi. Vomited nematodes must be differentiated from Toxocara canis, Toxocara cati, and Toxascaris leonina.
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Human Health Significance: Physaloptera spp. of dogs and cats are not considered a zoonosis.
Spirocerca lupi Infection
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Cause: Spirocerca lupi (esophageal worm), Superfamily Spriuroidea, Order Spirurida.
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First Described: Karl Asmund Rudolphi (Swedish parasitologist and “father” of helminthology), 1809.
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Affected Hosts: Domestic dogs, wild canids, and other carnivores; rarely cats.
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Geographic Distribution: Worldwide but primarily in tropical and subtropical regions with the highest prevalence in the southern United States, Brazil, the Caribbean, South Africa, and the Middle East.
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Route of Transmission: Dogs become infected after ingestion of the intermediate host (coprophagous beetles in the Family Scarabaeidae, Order Coleoptera) or paratenic hosts (e.g., birds, frogs, lizards and other reptiles, rodents) containing a third-stage larva.
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Major Clinical Signs: Vomiting or regurgitation, odynophagia, ptyalism, respiratory difficulty, cough, weight loss, and fever.
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Differential Diagnoses: Differentials for regurgitation include esophageal foreign bodies, esophageal strictures, esophageal neoplasia or granulomas of other origin, megaesophagus, and so on. Differentials for vomiting include any GI or systemic cause of chronic vomiting (e.g., idiopathic gastritis, gastric foreign body, gastric neoplasia, food intolerance/allergy, chronic pancreatitis). Eggs must be differentiated from Physaloptera spp.
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Human Health Significance: Spirocerca lupi infection is not considered a zoonosis.
Strongyloides spp.
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Cause: Strongyloides are commonly referred to as threadworms and belong to the Family Strongyloididae in the Order Rhabditida.
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First Described: Larval stages of Strongyloides stercoralis were first isolated from human feces in 1876; the first identification of natural infection in a dog was in 1914. In cats, Strongyloides planiceps was isolated by Leiper from a rusty tiger cat (Felis planiceps) in 1927. Strongyloides felis was first isolated from cats in India in 1925. While Strongyloides tumefaciens was first noted in cats in the USA in 1929, it was not described or named until 1941.
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Affected Hosts: Strongyloides stercoralis occurs in dogs, cats, non-human primates, and people. Strongyloides felis and S. tumefaciens have been described in domestic and wild cats; S. planiceps in domestic and wild cats, dogs, and wild carnivores.
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Geographic Distribution: Worldwide.
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Route of Transmission: Oral, percutaneous, and, less frequently, transmammary infections occur in dogs. Oral and percutaneous transmission occur in cats.
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Major Clinical Signs: Subclinical infections are common. Cough and other signs of bronchial involvement can occur in the early stage of infection in dogs. Severe enteritis with profuse diarrhea can occur in the later stage of infection. Skin papules are sometimes seen when larvae enter the dog percutaneously. In cats, clinical signs are rare, but diarrhea has been reported in some infections.
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Differential Diagnoses: The clinical signs are nonspecific and must be differentiated from other causes of diarrhea, for example, dietary, infectious, inflammatory, toxic, or extraintestinal causes of diarrhea. In puppies, S. stercoralis must be differentiated from other parasites that have larval lung migration stages (e.g., Toxocara canis, Ancylostoma caninum), cause diarrhea, and are able to enter the animal percutaneously (e.g., Ancylostoma caninum, [Uncinaria stenocephala]). In cats and dogs, recovered larvae must be distinguished from lungworm and hookworm larvae.
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Human Health Significance: Strongyloides stercoralis can be transmitted from dogs to people and from people to dogs. Zoonosis of cat Strongyloides has not been studied and there have been no reports of Strongyloides being transmitted from cats to people.
Mammomonogamus spp.
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Cause: Mammomonogamus ierei and Mammomonogamus auris, which occur in cats, are commonly referred to as gapeworms. These nematodes belong to the Family Syngamidae.
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First Described: Mammomonogamus ierei (synonym Syngamus ierei) was first described by Buckley in 1934, who isolated it from a domestic cat in Trinidad. Mammomonogamus auris (synonym Syngamus auris) was first described by Faust and Tank in 1934, who isolated it from the middle ear of several cats in China.
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Affected Hosts: Mammomonogamus ierei and M. auris infect domestic cats.
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Geographic Distribution: The distribution of Mammomonogamus is disparate with M. ierei reported in the Caribbean and M. auris found in Asia.
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Route of Transmission: Unknown. Given the life cycle of other parasites in this family, it is likely that paratenic hosts are involved.
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Major Clinical Signs: Subclinical infections are common. However, infections can be associated with inflammation of the nasopharynx resulting in a mucoid nasal discharge, coughing, sneezing episodes, and weight loss with M. ierei. Head shaking has been seen in a cat with M. auris infection.
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Differential Diagnoses: Other infections that cause nasal discharge and sneezing (e.g., viral infections, Eucoleus aerophilus, Cuterebra spp.). In the case of M. auris, Otodectes cynotis also can result in head shaking. The dark cerumen associated with O. cynotis infection does not occur with M. auris infection. Eggs of M. ierei and M. auris can be seen in a fecal flotation.
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Human Health Significance: There are no reports of M. ierei and M. auris infecting humans and neither are believed to be zoonotic.
Dioctophyme renale
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Cause: Dioctophyme renale, the giant kidney worm, is the largest parasitic nematode of domestic animals (Family Dioctophymidae and the Order Ascaridida).
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First Described: Dioctophyme renale was first described by the German zoologist Johann Goeze in 1782; earlier reports of giant kidney worms date back to the late 1500s.
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Affected Hosts: Most cases of D. renale in domestic animals are reported in dogs, with infections occasionally seen in cats and other host species, including humans. Fish-eating vertebrates, especially mink and other mustelids, are the natural definitive host.
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Geographic Distribution: Dioctophyme renale has a sporadic, worldwide distribution although reports of infection are rare in Africa and Asia. The parasite is widespread in the Americas and has been reported from dogs and other hosts from Canada to Brazil.
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Route of Transmission: Eggs are shed in the urine of infected definitive hosts. First-stage larvae develop inside the eggs and hatch following ingestion by aquatic oligochaete annelid intermediate hosts found in the detritus of ponds and streams. Third-stage larvae develop within the tissues of the annelids and may be passed to paratenic hosts, such as fish and frogs, when they ingest the intermediate hosts. Dogs and other final hosts are infected upon ingestion of annelids, or, more commonly, by ingesting third-stage larvae in fish paratenic hosts.
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Major Clinical Signs: Most infections are subclinical. Some dogs have hematuria, renal pain, renal enlargement, abdominal pain, and abdominal effusion. Development of worms in subcutaneous fat has also been reported.
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Differential Diagnoses: Other causes of cystitis; renal neoplasia; or a retroperitoneal, abdominal, or subcutaneous mass. Abdominal D. renale infection in cats can resemble FIP. Eggs of D. renale are not always present in urine sediment and thus diagnosis may sometimes be made by ultrasound or exploratory laparotomy.
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Human Health Significance: Although rare, zoonotic infections with D. renale have been reported and are associated with ingestion of larvae in undercooked fish or frogs.
Dracunculus insignis
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Cause: Dracunculus insignis, a subcutaneous worm of raccoons and other carnivores that also infects dogs, is a spirurid nematode closely related to the human Guinea worm, Dracunculus medinensis.
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First Described: Dracunculus spp. have been described since antiquity. Dracunculus medinensis was described by Linnaeus in 1758, and D. insignis by Leidy in 1858.
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Affected Hosts: Most cases of D. insignis infection in domestic animals are reported in dogs, although ferrets are also susceptible; a limited number of cases have been described in cats. Wild carnivores, especially raccoons, are most commonly infected and considered the natural definitive host of this parasite in North America. Although primarily a human parasite, D. medinensis also readily infects dogs in endemic areas.
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Geographic Distribution: Dracunculus insignis has only been reported from Canada and the United States. Due to concerted eradication efforts, D. medinensis is currently limited to three countries in Africa. Other Dracunculus spp. have been reported from mammals, snakes, and turtles in the Western Hemisphere and from snakes in Europe, Africa, Asia, and Australia.
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Route of Transmission: Gravid female Dracunculus spp. migrate to the extremities of the definitive host and form subcutaneous cysts. The presence of the nematode induces the formation of blisters; when immersed in water, the uterus of the nematode ruptures, releasing hundreds of thousands of larvae into the water. The motile larvae are ingested by copepod intermediate hosts. After third-stage larvae develop, copepods are ingested by definitive hosts drinking water; the nematodes then migrate to subcutaneous locations, mature, mate, and eventually form new cysts to continue the life cycle. Alternatively, infected copepods may be ingested by aquatic vertebrates which can then serve as paratenic hosts.
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Major Clinical Signs: Dogs with D. insignis present with fluctuant subcutaneous swellings, usually on a distal extremity or, less commonly, the thorax. Lesions are often pruritic and painful. The skin may appear ulcerated or bear a patent opening; when the affected limb is immersed in water, an adult nematode may emerge.
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Differential Diagnoses: Other, more common causes of subcutaneous masses include lipoma, reactive lymph nodes, neoplasia, or other dermal parasites (e.g., Cuterebra, Dirofilaria repens). However, the distinct location on a distal extremity and, when present, the appearance of a patent ulcer through which a nematode emerges, considerably narrows potential diagnoses. Specimen collection using fine-needle aspiration often leads to recovery of D. insignis larvae. Long female nematodes may be encountered during surgical exploration of the cystic lesion.
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Human Health Significance: Human infection is most commonly by D. medinensis. Recent reports of D. medinensis in domestic dogs have created challenges in the final stages of eradication efforts for the human Guinea worm.
Ocular Nematodes
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Cause: Onchocerca lupi and Thelazia spp. Aberrant migration has also resulted in other species of nematodes reported from the eye, including Dirofilaria spp., Dracunculus spp., and Toxocara spp.
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First Described: Onchocerca lupi was first described in a feral wolf in Russia. Thelazia callipaeda was first described by Ralliet and Henry in 1910 and Thelazia californiensis by Price in 1930.
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Affected Hosts: Onchocerca lupi is primarily a parasite of domestic dogs although feline onchocerciasis has been reported. Thelazia callipaeda and T. californiensis are described from dogs and cats with occasional reports from wildlife definitive hosts. Other Thelazia spp. infect the eyes of large animals.
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Geographic Distribution: Ocular nematodes occur sporadically around the world, with O. lupi reported from northern Asia, southern and central Europe, and the southwestern United States; T. callipaeda from Asia and, more recently, Europe; and T. californiensis from western North America.
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Route of Transmission: The life cycle of O. lupi is not fully understood, but other Onchocerca spp. are transmitted between definitive hosts by arthropod intermediate hosts, including black flies (Simulium spp.) and biting midges (Culicoides spp.). Thelazia spp. are transmitted by muscid flies feeding around the eyes.
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Major Clinical Signs: Ocular lesions due to O. lupi and Thelazia spp. may be mild to severe although many animals appear largely subclinical. In the acute phase of O. lupi infection, general ocular discomfort is seen with excessive lacrimation and photophobia. In chronic infections, nodules develop on the sclera, conjunctiva, and eyelids. Infection with Thelazia spp. may be associated with chronic conjunctivitis but nodules are not present.
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Differential Diagnoses: Many infectious, inflammatory, and traumatic conditions can cause ocular irritation and conjunctivitis. However, once nematodes are visualized coiled in inflammatory tissue on the conjunctiva (O. lupi) or free under the eyelids or nictitating membrane (Thelazia spp.), the diagnostic list of differentials is short. Other nematodes that occasionally migrate aberrantly to the eyes include Angiostrongylus vasorum, Dirofilaria spp., Dracunculs insignis, Toxocara spp., and Trichinella spiralis (eyelid).
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Human Health Significance: Human infection with both O. lupi and Thelazia spp. occasionally occurs resulting in ocular irritation, excessive lacrimation, and the presence of intraocular nematodes.
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Efficacy of ivermectin to control Strongyloides stercoralis infection in sheltered dogs
2019, Acta TropicaCitation Excerpt :In immunocompromised patients the parasites can disseminate to visceral organs and tissues, a condition known as ‘disseminated strongyloidiasis’ (Viney and Lok, 2015). Clinical signs of canine strongyloidiasis range from mild to severe, mostly in young (Ferreira et al., 2006) and adult sheltered dogs (Paradies et al., 2017) whereas larval dissemination has been documented only in experimental conditions (Genta et al., 1986, Grove et al., 1983). A combination of serological and parasitological tests is suggested for the diagnosis of human infection (Buonfrate et al., 2015; Bisoffi et al., 2014).
In dogs, information on treatments against S. stercoralis infection is rare and anecdotal. The aim of the present work was to evaluate the treatment outcome of S. stercoralis natural infection in sheltered dogs. Furthermore, based on the potential risk of infection, people working in the infected shelter were also tested. Seventeen sheltered dogs positive to S. stercoralis using the Baermann test were treated with ivermectin 200 μg/kg/sid/os for two consecutive days. Only two dogs showed clinical signs suggestive of strongyloidiasis (diarrhea, weigh loss) at diagnosis. All dogs showed consistently negative results for S. stercoralis at weekly monitoring after treatment using both the direct microscopy and Baermann test. Real-time PCR confirmed negative results at the last follow up 2 months after treatment. Serology performed at the first diagnosis showed that 82% and 41% of dogs were positive for S. stercoralis using an IFAT (titres ranging from 1:40 to 1:320) and ELISA, respectively. Two months after treatment, IFAT titres were strongly reduced in all animals. The results of clinical pathological laboratory tests at diagnosis in the positive dogs were within normal ranges, except for the two symptomatic dogs. Serum collected from two out of 14 shelter workers tested positive with titres 1:20 and 1:40 for S. stercoralis using an IFAT. Results of the study confirm that ivermectin was an effective treatment option to control S. stercoralis infection in dogs. Shelter workers are at risk of infection with S. stercoralis, thus the application of correct deworming protocols to reduce the environmental infective larval burden is essential to protect dogs and probably also shelter workers from the risk of infection.
Nematoda
2019, Parasiticide Screening: Volume 2: In Vitro and In Vivo Tests with Relevant Parasite Rearing and Host Infection/Infestation MethodsEvaluation of strongyloidiasis in kennel dogs and keepers by parasitological and serological assays
2007, Veterinary ParasitologyStrongyloides stercoralis is an intestinal nematode with worldwide distribution, particularly in tropical and subtropical regions. Due to the low sensitivity of traditional parasitological methods, the detection of serum specific antibodies may serve as an alternative test for the diagnosis. The aims of the present study were to verify the occurrence of S. stercoralis and the presence of specific IgG antibodies to the parasite in kennel dogs and keepers, using parasitological and serological assays. A total of 181 dogs were examined from 7 breeding kennels in the city of Uberlândia, southeastern region of Brazil and distributed as follows: kennel A (n = 41), kennel B (n = 16), kennel C (n = 11), kennel D (n = 63), kennel E (n = 11), kennel F (n = 18) and kennel G (n = 21). Fecal and serum samples from 11 keepers responsible for kennel cleaning and dog control were also collected in five of the seven kennels (two from kennel A, one from kennel B, four from kennel D, two from kennel E and two from kennel G). Overall, enteroparasites were detected by parasitological assays in 66, 36.5% (95% CI: 2.5–43.4%) of the 181 dogs tested. Only one (0.6%) dog was copropositive for S. stercoralis. Among the keepers only one fecal sample, 9.1% (95% CI: 8.6–9.4%) was positive for hookworm by the Lutz method. Serological assays showed that 44 (24.3%) of the 181 dogs were seropositive for S. stercoralis in at least one of the tests in the following kennels: 21 (11.6%) in kennel A; 1 (0.6%) in kennel B; 5 (2.7%) in kennel C; 6 (3.3%) in kennel D; 1 (0.6%) in kennel E; 9 (4.9%) in kennel F and 1 (0.6%) in kennel G. Among the keepers no S. stercoralis seropositive samples were identified using IFAT but 2 (18.2%) of the keepers from kennel D and 1 (9.1%) from kennel G were seropositive by ELISA. The present study demonstrated that the occurrence of S. stercoralis infection in kennel dogs and keepers is low in the city of Uberlândia and that serological assays can contribute to the diagnosis of canine as well as human strongyloidiasis.
Parasitological and serological diagnosis of Strongyloides stercoralis in domesticated dogs from southeastern Brazil
2006, Veterinary ParasitologyCanine strongyloidiasis is a parasitic infection caused by the nematode Strongyloides stercoralis and presents a great zoonotic potential. Its confirmation, using coproparasitological methods, is difficult. The detection of serum specific antibodies, however, may facilitate the diagnosis. The aims of this study were to determine the presence of S. stercoralis through the use of parasitological methods and to detect specific antibodies to the parasite in serum samples from domestic dogs by using the indirect fluorescent antibody test (IFAT) on slides and the enzyme-linked immunosorbent assay (ELISA). A total of 215 dogs of various breeds, from the cities of Uberlândia, Araxá and Campo Belo in the State of Minas Gerais, were examined and distributed according to age into the following groups: (I) 19 males and 20 females of 1–2 months old; (II) 11 males and 20 females of 2-month- to 1-year-old and (III) 41 males and 104 females, from 1 to 7 years old. Coproparasitological results showed that 63/215 (29.3%) of the dogs presented some kind of parasite, with two (0.9%) dogs (one from Araxá and the other from Uberlândia) passing S. stercoralis larvae in the feces. Serological results revealed antibodies to S. stercoralis in 45/215 (20.9%) of the dogs, with seropositivity rates of 0% (0/39) in Group I, 22.6% (7/31) in Group II, and 26.2% (38/145) in Group III. No serological cross-reactivity between S. stercoralis and hookworms or Ascaridae was found. Hookworm infections were seen in 31 dogs, but only one of these dogs (infected with both hookworm and Cystoisospora spp.) was S. stercoralis seropositive by IFAT. The present study demonstrated, for the first time, natural S. stercoralis infections in dogs diagnosed by coproparasitological and serological methods. It was concluded that the detection of specific antibodies to S. stercoralis by IFAT and ELISA may contribute to the diagnosis of canine strongyloidiasis.
How do host immune responses affect nematode infections?
2002, Trends in ParasitologyHost immune responses limit, and in some instances eliminate, nematode infections. There is considerable interest in enhancing these natural processes by the use of antinematode vaccines to achieve control of infection or disease. How nematodes are damaged is unclear. Worms might be damaged directly by effector cells and molecules of the immune system. Alternatively, they might be damaged by the physiological stress of their efforts to resist attack. Separating these possibilities could have important implications for approaches to the control of nematode infections and the disease that they cause.