Report of rare case of intense parasitism by 34 specimens of Dioctophyme renale in a dog

Braz J Vet Parasitol 2020; 29(4): e011820 | https://doi.org/10.1590/S1984-29612020080 This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Report of rare case of intense parasitism by 34 specimens of Dioctophyme renale in a dog

Dioctophyme renale (Goeze, 1782) is a nematode that causes dioctophymosis, a parasitic disease of chronic nature. This parasitosis develops through an indirect biological cycle and affects wild animals, domestic animals and humans. Infection occurs through ingestion of infective larvae that are present in the intermediate host (Lumbriculus variegatus) or in paratenic hosts (fishes and frogs) (Mace & Anderson, 1975). The right kidney is the organ mostly affected by this disease, which leads to destruction of the renal parenchyma, with consequent loss of organ function (Measures, 2001;Pedrassani & Nascimento, 2015).
The erratic cycle of D. renale may facilitate the finding of parasites in other anatomic regions. Case reports describe the finding of the nematode free in the abdominal cavity (Paras et al., 2018;Butti et al., 2020), left kidney (Perera et al., 2017b), mammary gland (Paras et al., 2018), prostate (Butti et al., 2020) and abdominal musculature (Caye et al., 2018) The clinical signs presented by animals affected by this parasitic disease are variable, and clinical signs include apathy, progressive weight loss, hematuria (Radman et al., 2017), ascites and abdominal pain (Measures, 2001). However, clinical signs are often unapparent (Mesquita et al., 2014;Pedrassani et al., 2017). Drugs are ineffective for controlling the disease, and it can only be treated surgically, through nephrectomy of the parasitized kidney or direct removal of the parasite (Pedrassani & Nascimento, 2015). The aim of this study was to describe a case of a dog with high parasitic load of helminths of the species D. renale.
A five-year-old female dog of the Bull Terrier breed was attended at the Veterinary Hospital of the Federal University of Pelotas, because it presented a swollen abdomen that had been evolving for 20 days and progressive weight loss. The patient was dehydrated, with pale-pink mucosae, and was tachypneic and tachycardic. From abdominal ultrasonography, a diagnosis of renal dioctophymosis with dissemination in the abdominal cavity was made. In addition, the patient presented peritonitis, edematous mesentery and a moderate quantity of free fluid.
Laboratory analyses revealed anemia (Hb 8.8 g.dL -1 ; Hct 26.5%), hypoalbuminemia (2.29 g.dL -1 ), hematuria, leukocyturia and presence of D. renale eggs in the urine. The serum biochemical tests showed that the levels of creatinine (1.0 mg.dL -1 ) and urea (43.23 mg.dL -1 ) were within the normal range for dogs. After evaluation and stabilization, the patient was sent for the surgical procedure of exploratory laparotomy and right nephrotomy for the treatment of the disease.
Several specimens of free D. renale were removed from the abdominal cavity and from inside the right kidney, which presented perforation of its capsule, thus enabling translocation of the parasites. Parasites were found in the upper right abdominal quadrant, in the right lateral and hypochondriac regions, in the kidney and liver and in body fluids containing blood, in moderate quantity. The omentum was reactive, with proliferative areas adhering to the liver, stomach, small and large intestines, pancreas, spleen, urinary bladder and internal abdominal wall.
In total, 34 parasite specimens were removed, among which 27 were free in the abdominal cavity and seven were inside the right kidney ( Figure 1). The parasites were identified according to their sizes, coloration, anterior extremity with hexagonal mouth without lips and posterior extremity with a copulatory bursa in the males and an obtuse tail in the females (Pedrassani & Nascimento, 2015;Butti et al., 2018). All of them presented normal coloration and presence of intense motility. There were 11 females and 16 males in the abdominal cavity (Figure 2), and all the seven parasites in the right kidney were female. While the free-living females in the abdominal cavity had a mean length of 56.45 cm (range from 15 to 74 cm), those females in the kidney had a mean length of 42.57 cm (range from 39 to 45 cm). The males had a mean length of 24.93 cm, with a range from 21 to 30 cm. Samples were collected from the surface of each parasite using a sterile swab. These samples were sent for bacterial culturing in blood agar and MacConkey agar, and there was no growth of microbes in either of these. Histopathological analysis on fragments from the omentum revealed the presence of intense inflammatory infiltrate of lymphocytes, plasmacytes and macrophages. Very many eggs of D. renale, of rugose and bioperculate appearance, were found in the middle of the inflammatory connective tissue (Figure 3).
There have been reports of similar cases of multiparasitism caused by D. renale. In reports on dogs examined through necropsy, Monteiro et al. (2002) found 34 parasites (28 in the abdominal cavity and six in the right kidney) and Sadighian & Amini (1967) found 27 adult worms (14 in the right kidney, 10 in the peritoneal cavity and three in the peritoneum). Perera et al. (2017b) reported an in vivo finding of 23 parasites in the abdominal cavity in a single dog, which survived after removal of the nematodes.
The measurements of the 27 parasites described by Sadighian & Amini (1967) ranged from 29 to 75 cm among the females and from 21 to 33 cm among the males. Those sizes were similar to what was found in the present report, which shows that the high parasite load did not interfere with the development of the specimens encountered. In another report in the literature, it is stated that females can reach a length of 100 cm and males, 45 cm (Pedrassani & Nascimento, 2015).
The patient that was followed up in the present report had undergone a cesarean procedure, together with ovariohysterectomy, five months before receiving the diagnosis of dioctophymosis, performed by another professional. There were no reports of any macroscopic alterations seen during those procedures. Therefore, it can be suggested that the disease developed over that five-month period, since the prepatent period of D. renale in dogs is estimated to be 135 days (Mace & Anderson, 1975).
This dog was living in the rural zone of the municipality of Pelotas, in the south of the state of Rio Grande do Sul, Brazil. There have been several cases of animals parasitized by D. renale in the Pelotas region (Rappeti et al., 2017). Eggs of this parasite were found in soil samples from the urban region of the city (Perera et al., 2017a), and third-stage larvae were found in 50% (n = 60) of the specimens of the turtle D'Orbigny's slider (Trachemys dorbigni) that were evaluated (Mascarenhas & Müller, 2015). These surveys show that dioctophymosis is present and disseminated in Pelotas, thus favoring infection with large numbers of worms.
In the report by Monteiro et al. (2002), renal perforation was also found, which allowed passage of parasites. It can be suggested that the high parasite load inside the kidney may have led to dispersal of parasites out from the kidney to the abdominal cavity, given the limited physical space inside the kidney capsule. In addition, there is the possibility that the free worms in the abdominal cavity had perforated the kidney, given that there is a migratory tendency towards this organ (Hallberg, 1953;Mace & Anderson, 1975). Likewise, considering the anatomical characteristics of the host, migration of the parasites to the right kidney explains the finding that all specimens were observed to be in the right lateral region of the abdomen.
The absence of bacterial growth in the cultures that were performed demonstrated that the parasitosis was not accompanied by bacteria infection. Aseptic peritonitis occurred through mechanical factors, due to the high parasite load and the presence of eggs that had not been eliminated and were causing inflammation and irritation to the tissue (Anderson, 2000). Moreover, chemical factors are also involved, given that the parasites eliminate lipolytic and proteolytic esophageal enzymes, thus causing tissue lysis (Pedrassani & Nascimento, 2015). The tissue lesions explain the formation of connective tissue and the inflammatory reaction surrounding the eggs, as described by Measures & Anderson (1985).
We believe that this report presents the largest number of specimens of D. renale that have so far been removed from a single dog in vivo (34 specimens). We were unable to find any similar report in the current literature available through the main databases. It was noted that the high parasite load did not impede full development of the parasites, which had reached sexual maturity with elimination of eggs. This led to consequent peritonitis, abdominal inflammatory reaction and tissue destruction.
The patient was still in a clinical stable condition at the time of writing this report, 148 days after the surgical treatment. The creatinine levels remained stable on days 11, 14 and 36 post-surgery, with values of 1.4 mg.dL -1 , 1.3 mg.dL -1 and 1.2 mg.dL -1 . The urea concentrations progressively decreased (86.65 mg.dL -1 , 71.93 mg.dL -1 and 64.53 mg.dL -1 ) over these timepoints. Currently, the creatinine concentration is 1.9 mg.dL -1 and urea 97.0 mg.dL -1 . The patient continues to be clinically monitored.