Introduction

Stomach worm infections in dogs are considered uncommon; however, the true prevalence of infection in client-owned dogs is unknown.^1,2 These nematodes are classified within the genus Physaloptera, of which there are many recognized species worldwide infecting domestic dogs and cats, feral cats, coyotes, foxes, raccoons, bobwhite quail, and other nonmammalian species.^1–12 Although speciation is rarely performed in clinical cases, P rara is considered the most common stomach worm of domestic dogs and cats in the United States.^1,2,11 In all species, the nematode attaches primarily to the stomach, although attachment to the duodenum has also been reported.^1,2,11 In the domestic dog, infections may be silent; however, when clinical signs are present, chronic, intermittent vomiting, usually with a normal appetite, is most commonly reported.^1,2 Regurgitation was also reported as a clinical sign in a small number of dogs; however, there was no apparent significant esophageal disease identified in those dogs.^1,2

A diagnosis of Physaloptera infection in domestic dogs is difficult to establish for several reasons, not the least of which is silent infection. In dogs with clinical signs from infection, noninvasive identification of Physaloptera with fecal flotation is complicated by the fact that many infections tend to have a low burden (often <5 nematodes), females produce fewer eggs relative to other common parasitic infections, single-sex infections occur, and Physaloptera eggs are reported to have a specific gravity higher than most routinely used fecal flotation solutions.^2,13 Dogs rarely vomit the parasite, likely because of the firm attachment to the gastric mucosa. Endoscopic visualization is therefore necessary for confirming the vast majority of infections in dogs. Given the expense and variable availability of gastroscopy, it is generally recommended to presumptively treat for Physaloptera in dogs with chronic, intermittent vomiting and a normal appetite.^1,2 This is especially true for dogs with a history of ingesting the most common intermediate hosts for this parasite: grasshoppers, beetles, and cockroaches.²

Clinical signs from Physaloptera infection are believed to be a result of parasitic attachment to gastric mucosa, which creates mucosal disruption and erosion and subsequent inflammation.^1,2 However, gastritis is usually relatively mild histologically and is frequently absent in many cases.^1,2 Delayed gastric emptying has been reported in dogs with Physaloptera infection, although the mechanism for this is unknown.² There is no standardized treatment protocol for Physaloptera infections in dogs, although successful treatment with ivermectin, pyrantel pamoate, and fenbendazole (separately and in combination) have been reported.^1,2,14,15 However, Physaloptera may be more difficult to treat than other nematodes. Febantel and oxibendazole were reportedly ineffective at clearing Physaloptera at dosages sufficient to eliminate other common intestinal parasites.^16,17 Successful treatment is expected to resolve clinical signs in dogs, but reinfection with Physaloptera is common and may result in recurrent vomiting, which may be misinterpreted as treatment failure.^1,2

There is currently a limited number of retrospective studies and individual case reports of Physaloptera infections in dogs.^1,2,18–21 The aim of this retrospective study was to report the clinical presentation, response to various therapies, results of diagnostic testing, and outcome in dogs that were diagnosed via endoscopic visualization of Physaloptera.

Materials and Methods

Results

The 27 dogs ranged in age from 0.3 to 11.8 yr (median 3.4 yr) and ranged in weight from 2.5 to 41.5 kg (median 18.6 kg). There were 17 male (13 neutered) and 10 female (9 neutered) dogs. Breeds included Labrador retriever (n = 6 dogs), Yorkshire terrier (n = 2), dachshund (n = 2), and nine additional breeds represented by one dog each. There were eight dogs of mixed breed. More dogs presented during the months spanning October through January (n = 20 dogs), including 7 dogs in November. Three dogs were diagnosed from February through May, and four dogs from June through September.

The most common clinical sign attributed to gastric Physaloptera infection was chronic vomiting in 23 dogs. One dog had chronic diarrhea, and there were no clinical signs attributed to Physaloptera in three dogs with gastric or esophageal foreign bodies. In seven of the dogs with chronic vomiting, it could not be ascertained from the history whether the dogs were vomiting or regurgitating. Six of these seven dogs were reported to only be vomiting undigested food. In the 23 dogs with chronic vomiting, signs had been present from 10 days to 5 mo (median 1.2 mo). The frequency of vomiting was specifically noted in the medical record for nine dogs and ranged from four times daily to twice weekly. Vomiting was described as being postprandial in all 12 dogs for whom this information was recorded, but the timing ranged from 15 min to 8 hr (vomiting that occurred more than 2 hr after a meal was considered postprandial if it contained undigested food). The content of the vomitus was reported as undigested food in 11 dogs, with only 2 dogs reportedly vomiting bile. None of the dogs were reported to be vomiting water or have any change in appetite or thirst. In three dogs, Physaloptera was visualized during endoscopy for removal of gastric (n = 2 dogs) or esophageal (n = 1) foreign bodies, but no clinical signs were attributed to the parasite. One of these three dogs vomited a toy 3 wk earlier and had vomited daily for 10 days after that, but no vomiting had been noted in the 10 days prior to endoscopy or prior to vomiting the toy 3 wk earlier. One dog vomited a piece of a toy on the morning of presentation and had no other history of vomiting. The dog with the esophageal foreign body presented for gagging and hypersalivation of 1 day duration and had no history of chronic vomiting. One dog did not present for vomiting and had chronic small bowel diarrhea of 3 mo duration, which had been nonresponsive to dietary and antibiotic trials. No alternative diagnosis was obtained to explain the diarrhea in this dog.

Anthelmintic therapy had been administered by the primary care veterinarian prior to endoscopy for the presenting complaint of vomiting in eight dogs and failed to resolve vomiting in all eight dogs. Fenbendazole (50 mg/kg per os [PO] q 24 hr × 3 days) alone was given to three dogs 6 days to 5 wk prior to endoscopy. Fenbendazole (50 mg/kg PO q 24 hr × 5 days) in combination with pyrantel pamoate (8 mg/kg PO once) was given to one dog, and this dog was retreated with the same fenbendazole protocol with pyrantel pamoate at 26.5 mg/kg 7 wk later, which was 1 mo prior to endoscopy. One dog was administered praziquantel/pyrantel (dose not reported) 6 and 4 wk prior to endoscopy and praziquantel/pyrantel/febantel (dose not reported) 1 wk prior to endoscopy. Two dogs were treated once with pyrantel pamoate (dose not reported, 2 and 5 wk prior to endoscopy), and another dog was reportedly treated for presumptive Physaloptera infection less than 1 mo prior to endoscopy, but the regimen was not reported. Seven dogs were receiving Heartgard Plus^a and one dog was receiving Interceptor^b as a monthly heartworm preventive. One dog had been treated with a combination of fenbendazole (84 mg/kg once daily for 5 days) and pyrantel (8.4 mg/kg once and repeated in 2 wk) apparently successfully for presumptive Physaloptera infection four times, with no episodes of vomiting for 8, 14, 7, and 3 mo after each treatment. Upon the fifth recurrence of daily vomiting of undigested food, the dog was then referred to KSUVHC for a definitive diagnosis of Physaloptera infection.

Antiemetic therapy consisting of metoclopramide, maropitant, or ondansetron was administered to nine dogs. Metoclopramide was reported to be ineffective in the six dogs that received it. One of these dogs also had no response to ondansetron. Maropitant was administered to three dogs, two of whom showed no response and one that was reported to have a slight reduction in the frequency of vomiting episodes. Other therapies that had been attempted in these dogs to no effect prior to a definitive diagnosis included dietary trials (n = 9 dogs), various oral antibiotics (n = 8), famotidine (n = 5), prednisone (n = 1), and sucralfate (n = 1). Five dogs had no therapy prior to endoscopy.

A CBC and serum biochemistry profile were both performed in 23 dogs. The results of the CBC were normal in 19 dogs. In two dogs, mild thrombocytosis was present (622 and 705 K/μL (reference interval 200–500 K/μL). Mild lymphopenia was present in three dogs (0.63–0.78 × 10⁹/L; reference interval 0.80–4.3 × 10⁹/L). The results of the serum biochemistry profile were normal in 21 dogs. One dog that was later diagnosed with pituitary-dependent hyperadrenocorticism had an elevated serum alkaline phosphatase (17.20 μkat/L; reference interval 0.02–2.37 μkat/L) and serum cholesterol (13.86 mmol/L; reference interval 3.44–10.20 mmol/L). One dog had hyperglobulinemia (68 g/L; reference interval 13–32 g/L) and hypoalbuminemia (23 g/L; reference interval 34–42 g/L). This dog had the most substantial worm burden. The eosinophil count in the 23 dogs for whom a CBC was performed ranged from 0 to 1.4 × 10⁹/L (median 0.40 × 10⁹/L; reference interval 0–1.5 × 10⁹/L). A baseline cortisol was evaluated in two dogs (34 and 80.2 nmol/L, respectively [reference interval 25–110 nmol/L]) and was deemed inconsistent with hypoadrenocorticism in both dogs. A qualitative fecal flotation was performed on five dogs using Sheather’s sugar solution (specific gravity between 1.24 and 1.27), three of whom were negative for parasites. One dog had Taenia spp. and one dog had Cystoisospora, Toxascaris, Physaloptera, and an unknown Capillaria on fecal flotation. One additional dog had a qualitative fecal flotation performed elsewhere (methodology unknown) that was reported to be negative for parasites.

Abdominal radiographs were performed on 14 dogs and abnormalities were described in only 5 dogs. In these five dogs, one had radiopaque foreign bodies (stomach and descending colon); one had inhomogeneous material distending the stomach (Figure 1), which was determined endoscopically to be a large worm burden; one dog had multiple small mineral opacities in the pylorus; hepatosplenomegaly was described in the dog with pituitary-dependent hyperadrenocorticism; and one dog had mild duodenal dilation and mixed gastric contents. One of the two dogs with a gastric foreign body was reported to have unremarkable abdominal radiographs. Thoracic radiographs were obtained in 11 dogs, including the 7 dogs for whom vomiting and regurgitation could not be distinguished from the history. All thoracic radiographs were considered unremarkable except in the dog with chronic cough, in which a diffuse bronchointerstitial pattern was described. An esophagram was performed in two of the seven dogs with suspected regurgitation and was normal in both dogs. Abdominal ultrasonography was performed in 14 dogs, with abnormalities described in only 4 dogs. A gastric wall mass was suspected in one dog but was eventually discovered to be a radiolucent foreign body. Two dogs were described as having thickened gastric folds in the area of the fundus. One patient had an area of focal thinning in the duodenal wall that appeared consistent with an area of ulceration, but this was not confirmed on endoscopy.

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All dogs had Physaloptera visualized endoscopically ranging in number from single to multiple worms too numerous to count. The majority of dogs (n = 21 dogs) had only 1–3 worms visualized, with 13 dogs having one worm seen (Figure 2). In four dogs, the worm burden was considered to be in excess of 10 worms. However, in two dogs, the worm burden was estimated to be in excess of 50 worms (Figure 3). This included the one dog whose worm burden was considered responsible for the radiographic appearance of inhomogeneous gastric contents. This dog also had hypoalbuminemia and hyperglobulinemia (described above). Physaloptera was considered the small phenotype in 22 dogs and large phenotype in 5 dogs. Both dogs with >50 worms had the large phenotype. Two dogs had Physaloptera found on a second gastroscopic procedure performed 7 mo and 5 yr later, respectively, for recurrence of vomiting. In the first dog, a single small Physaloptera was found both times. In the second dog, one large Physaloptera was found initially, but >10 small worms were found on the subsequent exam.

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The location of worms within the gastrointestinal tract was recorded for 20 patients. In 16 dogs, the worms were identified only within the body of the stomach. In three dogs, all of whom were infected with the large phenotype, worms were found throughout the stomach, including the pylorus, and also in the proximal duodenum (Figure 4). In the remaining dog, one worm was found in the body of the stomach and one in the duodenum, both of which were the large phenotype. Endoscopic visualization of the gastric mucosa revealed follicles in 13 dogs, which varied in number from few (<5 identifiable follicles in the vicinity of the worm; n = 6 dogs) to multiple (>5 follicles, identified in the region of worm attachment; n = 4; Figure 5A) to extensive (too numerous to count and extending in regions distant from identifiable worm attachment; n = 3; Figure 5B). One dog that had few follicles had large numbers of pinpoint hemorrhages throughout the pylorus. In 14 dogs, no gross lesions of the gastric mucosa were identified. Gastric and duodenal mucosal biopsies were obtained from 19 dogs. Histological lesions were identified in 14 dogs. Six dogs had only histological lesions of the stomach, which were mild in all dogs and described as lymphocytic (n = 3), lymphoplasmacytic (n = 2), or eosinophilic (n = 1). Five dogs had only histological lesions of the duodenum, which were mild in four and moderate in one and were described as lymphocytic (n = 2), lymphoplasmacytic (n = 1) or eosinophilic (n = 2; including the dog with moderate inflammation). Three dogs had lesions in both the stomach and duodenum, which were mild in all three and described as eosinophilic (n = 2) or lymphoplasmacytic (n = 1). Spiral bacteria consistent with Helicobacter sp. were identified histologically in eight dogs, four of whom had no histological lesions of the gastric mucosa. One dog had submucosal sporocysts on histological examination of the duodenal biopsies, consistent with Sarcocystis or Hammondia, but with no concurrent inflammation. In the 13 dogs with gastric follicles identified endoscopically, no biopsies were obtained in four, the stomach was histologically normal in five, and eosinophilic or lymphoplasmacytic gastritis was seen in two dogs each.

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After endoscopy was performed, 24 dogs received treatment for Physaloptera infection; however, no standard treatment was used. Eight dogs were treated with fenbendazole (75–89 mg/kg PO q 24 hr × 5 days) in combination with pyrantel pamoate (7.5–20 mg/kg PO once). Repeated dosing in 2–8 wk was recommended in all eight dogs. In one dog, there appeared to be an intention to treat with this regimen, but a dosing miscalculation resulted in a fenbendazole dose of only 18.5 mg/kg/day. One dog was treated with fenbendazole at 50 mg/kg PO for 3 days in combination with a single dose of pyrantel pamoate (9 mg/kg PO), but this treatment was not repeated. Seven dogs were treated solely with a single course of fenbendazole at 75 mg/kg PO once daily for 5 days (n = 2), 50 mg/kg PO once daily for 5days(n = 3), or 50 mg/kg PO once daily for 3 days (n = 2). Two dogs were treated solely with pyrantel pamoate (5 mg/kg and 20 mg/ kg, PO) once and not repeated. Two dogs were treated with ivermectin (200 mg/kg PO), one of whom had a repeat dose 3 wk later.

Follow-up was available from 11 dogs with vomiting. In six dogs, the follow-up was reported within 2–7 days of discharge from the hospital, and vomiting was reportedly resolved in all six dogs. Resolution was attributed to complete worm removal in five dogs (four of these five dogs received additional anthelmintic therapy after endoscopy, and one did not receive any) and ivermectin in a dog with a large worm burden and incomplete worm removal. Two dogs were seen several times over the course of 6 yr at KSUVHC with no additional vomiting. In four dogs, follow-up was obtained when vomiting recurred, but the dogs were asymptomatic for 1, 7, and 10 mo and 5 yr. Two of these dogs were treated for presumed recurrent Physaloptera infection, and vomiting resolved in both dogs. One dog had endoscopy performed at the first recurrence of vomiting 7 mo later, at which time Physaloptera was diagnosed again. This dog was treated seven more times over the following 12 mo for recurrent vomiting with fenbendazole (65 mg/kg PO q 24 hr × 5 days) and pyrantel pamoate (18 mg/kg PO once) with rapid resolution of vomiting each time. In one dog, vomiting recurred 5 yr later, at which time endoscopy was performed and re-infection with Physaloptera confirmed. This dog was treated 10 days prior to endoscopy with fenbendazole (50 mg/kg PO q 24 hr × 3 days) and pyrantel pamoate (20 mg/kg PO once) when vomiting recurred, which did not resolve the vomiting. After endoscopy, at which time only 8 of the >10 worms were removed, the dog was treated with fenbendazole at a higher dose (75 mg/kg PO q 24 hr × 5 days) and pyrantel pamoate (20 mg/kg PO), both of which were repeated in 3 weeks. Vomiting resolved with the first of these treatments.

Discussion

Physaloptera are described as ranging in size from 1 to 6 cm; however, in the present study, dogs were infected with two distinct phenotypes. The small phenotype was estimated to range in size from 1 to 2 cm and the large phenotype was estimated to range from 5 to 6 cm in length. No dog was simultaneously infected with both phenotypes, nor was an intermediate size ever identified in any dog. Both phenotypes of worms were seen within the stomach, but only the large phenotype extended into the proximal duodenum. The largest worm burdens tended to be the large phenotype, and most of the infections (20 of 21 dogs) that carried the lowest worm burden (1–3 worms) were the small phenotype. In previous retrospectives and case reports of Physaloptera infections in dogs in which a description of the size was noted, the worms are all described as the small phenotype.^1,18–20 Although the genus of the large phenotype was confirmed as Physaloptera by a parasitologist^c, speciation was not performed. A study on the ultrastructural characteristics of Physaloptera rara removed from the stomach of a cat reported that the males measured 2.5–2.9 cm in length and the females measured 2.7–4.1 cm in length.²² It is possible the large phenotype represents a distinct species of Physaloptera and not a variation in size or maturity of the same species.

In this study, only one dog had a fecal flotation performed that was positive for Physaloptera infection; however, fecal flotation was only performed on six dogs. In four dogs, a negative fecal flotation would have been expected given that only one (n = 3 dogs) or two (n = 1) were identified endoscopically. The dog with a positive fecal flotation had a large number (>10) of the small-phenotype worm, making unisex infection unlikely. The remaining dog with a negative fecal flotation had >50 of the large-phenotype worm present on endoscopic examination. Because a unisex infection was unlikely in this dog, possible explanations are that the large-phenotype worms are nonreproductive, that they have a dramatically lower fecundity as compared with the small phenotype, or that the eggs are denser than those of the small-phenotype worm and unlikely to be recovered on routine fecal flotation. This difference could also support that the small and large phenotypes represent different species of Physaloptera.

The most commonly reported clinical sign in patients infected with Physaloptera in this study, similar to previous case reports, was chronic vomiting.^1,2,18–21 Although the description of expulsion of food was most consistent with regurgitation in seven dogs, there was a lack of radiographic or endoscopic evidence of esophageal disease in any of these dogs, suggesting that a passive form of vomiting was the cause of the clinical signs in these dogs. Six of these seven dogs had evidence of gastritis histologically, including all three dogs with eosinophilic gastritis. Although dysmotility could be a consequence of gastritis, only 9 of 19 gastric biopsies showed gastritis. It is also possible that dysmotility is related to a direct parasite-mediated effect. One dog in the current study had small bowel diarrhea as the sole clinical sign and was found to have more than 50 large-phenotype worms present within the stomach and duodenum. As this dog had no histological abnormalities identified on mucosal biopsies and no other identifiable cause for the diarrhea, the diarrhea may have been a manifestation of dysmotility induced by the parasite. Studies investigating the effect of Physaloptera on gastrointestinal motility have not been reported in the literature.

Clinical signs were resolved in all 11 patients for whom follow-up was received. Of these 11 patients, 9 were confirmed to have had all worms removed endoscopically prior to receiving treatment, and immediate resolution of clinical signs was likely a direct result of the removal of worm(s). The current treatment protocol recommended by one author (K.R.H.) includes a combination of fenbendazole (75 mg/kg PO q 24 hr × 5 days) and pyrantel pamoate (7.5 mg/kg PO once), with this combination repeated 3 wk after completion. Two dogs with resolution of clinical signs had a large enough worm burden that they could not all be removed endoscopically. One of these dogs was treated with the recommended protocol and the other with ivermectin.

Prior to undergoing endoscopy, eight dogs in this study received empirical anthelmintic therapy prior to endoscopic examination. Two of these dogs also received Heartgard Plus monthly. Six additional dogs that were not treated empirically with anthelmintic therapy received Heartgard Plus (n = 5 dogs) or Interceptor (n = 1) monthly. Clinical signs did not resolve or abate in seven of the dogs treated empirically or following the monthly administration of preventive in the other six dogs, suggesting therapeutic failure. The empirical anthelmintic therapy met or exceeded the recommended protocol described above in one dog only, who received this protocol four times with remission times ranging from 3 to 14 mo. The owner of this dog elected to have endoscopy performed to confirm the diagnosis of Physaloptera infection with the fifth episode. The long duration of remission following therapy in this dog supported reinfection, which was also consistent with the owner-reported history of frequent dietary indiscretions.

Theisen et al. reported the successful use of lower doses of pyrantel and/or fenbendazole than the above-recommended protocol, but they also removed all worms that were visible endoscopically.¹ Campbell and Graham recommended pyrantel pamoate at 20 mg/kg to treat suspected Physaloptera infections prior to performing endoscopy.² However, one dog in the current study was treated with pyrantel pamoate at 26.5 mg/kg on two occasions 7 wk apart, which failed to resolve vomiting either time, necessitating endoscopy. The authors believe that the above-described combination of fenbendazole (75 mg/kg PO q 24 hr for 5 days) and pyrantel pamoate (7.5 mg/kg PO once) is necessary to ensure elimination of Physaloptera infections in dogs.

Conclusion

Physaloptera infection should be considered for any dog with chronic, intermittent vomiting in the presence of a normal appetite, even in the face of prior administration of standard doses of anthelmintics or the use of monthly preventives, as well as a negative fecal flotation. A higher dose and longer course of fenbendazole in combination with pyrantel pamoate is recommended for treatment of confirmed or suspected Physaloptera infection.