Ultrasonographic, computed tomographic, and operative findings in dogs infested with giant kidney worms (Dioctophyme renale)

Sheila C. Rahal Department of Veterinary Surgery and Anesthesiology, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Maria J. Mamprim Department of Radiology and Animal Reproduction, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Hugo S. Oliveira Department of Radiology and Animal Reproduction, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Luciane R. Mesquita Department of Veterinary Surgery and Anesthesiology, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Luis G. Faria Department of Veterinary Surgery and Anesthesiology, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Regina K. Takahira Veterinary Clinic, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Lídia M. Matsubara Department of Veterinary Surgery and Anesthesiology, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Felipe S. Agostinho Department of Veterinary Surgery and Anesthesiology, School of Veterinary Medicine and Animal Science, Universidade Estadual Paulista (UNESP), Botucatu, SP, Rubião Júnior s/n, 18618970, Brazil.

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Abstract

Objective—To compare ultrasonographic, CT, and surgical findings in dogs infested with giant kidney worms (Dioctophyme renale).

Design—Case series.

Animals—15 crossbred dogs infected with D renale.

Procedures—Immediately after ultrasonography was performed with dogs in dorsal recumbency, sequential transverse images of the abdomen were acquired with a helical CT scanner. After plain CT, contrast CT was performed with a nonionic iodinated contrast agent. Subsequently, exploratory celiotomy was performed.

Results—In the corticomedullary area of the right kidney of 12 dogs, ultrasonography revealed several ring-like structures with an echogenic wall and anechoic central area in the transverse plane and arrayed as bands in the longitudinal plane. Similar structures were observed in the abdominal cavity of 10 dogs. In 13 dogs, CT revealed loss of corticomedullary differentiation in the right kidney, with discrete uptake of contrast material in the periphery of the kidney, and several ring-like or elongated structures with a hyperdense wall and hypodense center. In 11 dogs, the same structures were observed free in the abdominal cavity. Surgery revealed that 13 dogs had a damaged right kidney that required nephrectomy. Parasites were found free in the abdominal cavity of 7 dogs.

Conclusions and Clinical Relevance—Ultrasonography and CT were effective imaging methods for detecting D renale in the kidney and less effective for detecting parasites in the abdominal cavity. Care should be taken to avoid erroneously interpreting normal structures as parasites, especially in the abdominal cavity.

Abstract

Objective—To compare ultrasonographic, CT, and surgical findings in dogs infested with giant kidney worms (Dioctophyme renale).

Design—Case series.

Animals—15 crossbred dogs infected with D renale.

Procedures—Immediately after ultrasonography was performed with dogs in dorsal recumbency, sequential transverse images of the abdomen were acquired with a helical CT scanner. After plain CT, contrast CT was performed with a nonionic iodinated contrast agent. Subsequently, exploratory celiotomy was performed.

Results—In the corticomedullary area of the right kidney of 12 dogs, ultrasonography revealed several ring-like structures with an echogenic wall and anechoic central area in the transverse plane and arrayed as bands in the longitudinal plane. Similar structures were observed in the abdominal cavity of 10 dogs. In 13 dogs, CT revealed loss of corticomedullary differentiation in the right kidney, with discrete uptake of contrast material in the periphery of the kidney, and several ring-like or elongated structures with a hyperdense wall and hypodense center. In 11 dogs, the same structures were observed free in the abdominal cavity. Surgery revealed that 13 dogs had a damaged right kidney that required nephrectomy. Parasites were found free in the abdominal cavity of 7 dogs.

Conclusions and Clinical Relevance—Ultrasonography and CT were effective imaging methods for detecting D renale in the kidney and less effective for detecting parasites in the abdominal cavity. Care should be taken to avoid erroneously interpreting normal structures as parasites, especially in the abdominal cavity.

Giant kidney worms (Dioctophyme renale) are parasitic roundworms reported most often in dogs1–9 and wild carnivores10,11 and less frequently in cats,12 rats,13 and humans.14–16 The life cycle of the parasite requires an oligochete annelid intermediate host (aquatic oligochete annelids, terrestrial segmented worms, or earthworms), paratenic host (fish and frogs), and definitive host, which acquire the disease most commonly by ingestion of raw fish or frog or infested oligochetes.10,17 The prepatent period is approximately 155 days, but completion of the cycle may require up to 2 years.17

Although the predilection site for D renale in dogs is the right kidney, this parasite has also been found free within the abdominal cavity and less frequently at other sites, including the urinary bladder, uterus, inguinal area, and mammary gland.1–4,6,8,9,18–21 The renal parenchyma is progressively destroyed, leaving only a capsule containing the parasite and hemorrhagic exudate.1,3,17,18 Although some cases are subclinical, clinical signs may include hematuria, hyporexia, pollakiuria, anemia, emaciation, urinary tract infection, and peritonitis.1,2,4,6–9,12,17–19,22

Diagnosis is most commonly accomplished by finding ova in the urine, which will be detected only if there is a gravid female parasite in the kidney.1,5,7,9,17,18,22 However, in numerous studies,1–4,6,12 the diagnosis has been based on necropsy findings. Ultrasonography has been used to confirm the presence of the parasite in the renal parenchyma or uterus in some cases in dogs5,7,9,19–21 and in a monkey with an abdominal cyst.11 The methods used in human cases have included ultrasonography, CT,15,16 and MRI.14 Therefore, the purpose of the study reported here was to compare ultrasonography, CT, and surgical exploration for diagnosis of infection with D renale in dogs.

Materials and Methods

Animals—Fifteen crossbred dogs (6 males and 9 females), of ages from approximately 4 to 96 months (mean ± SD age, 33.1 ± 20.6 months) and weighing 1.75 to 13.75 kg (3.86 to 30.31 lb; mean ± SD, 8.03 ± 3.25 kg [17 ± 7 lb]) were included in the study. The dogs were owned by a nongovernmental organization and were referred to the veterinary hospital because of suspicion of dioctophymosis (D renale infestation). Two dogs had previously undergone surgery; however, there was a suspicion that some parasites had not been removed. The other 13 dogs were apparently subclinically affected, but other dogs from the same property had dioctophymosis. Urinalysis and CBC were performed on all dogs.

Imaging—Food was withheld from all dogs for 12 hours, and water was withdrawn 2 hours before premedication. To perform the abdominal ultrasonography examination (B-mode scan),a the dogs were premedicated with morphine (0.5 mg/kg [0.23 mg/lb], IM) and positioned in dorsal recumbency. Immediately after this procedure, general anesthesia was induced with propofol (5 mg/kg [2.3 mg/lb], IV) and maintained with isoflurane in oxygen to perform CT scanning. Sequential transverse images of the abdomen were acquired on a helical scannerb with the dogs positioned in dorsal recumbency. After plain CT, contrast CT was performed with a bolus injection of nonionic iodinated contrast agent (2 mL of iopromide/kg [0.9 mL/lb], IV). The scanning parameters were as follows: voltage peak, 120 kV; current, 130 mA; pitch, 2:0; and rotation time, 1 s/rotation. A slice thickness of 7 mm was used for plain CT and late-phase contrast CT of the entire abdomen. A slice thickness of 1 mm was used for contrast evaluation of the kidneys. Seven-millimeter slice thickness was used for the abdominal CT scan during the late-phase contrast study. For both imaging procedures, the damaged kidney was evaluated by scoring in points, depending on the degree of tissue damage: normal (0) = normal corticomedullary differentiation, absence of parasites, and normal renal contrast uptake on CT; low level of morphological alteration (1) = effacement of the medullary anatomic details, presence of parasites, and uptake of contrast material in the cortex on CT; medium level of morphological alteration (2) = effacement of medullary anatomic details, partial effacement of cortical anatomic details, presence of parasites, and heterogeneous uptake of contrast material in the cortex on CT; and high level of morphological alteration (3) = complete effacement of the capsular, cortical, and medullary anatomic details; kidney completely occupied by parasites; and heterogeneous uptake of contrast material in the kidney periphery on CT. Infestation of the abdomen and a kidney damaged by D renale were scored as absent or present. Evaluations were performed by an experienced radiologist.

Surgical procedures—Two or 3 days after imaging studies, exploratory celiotomy was performed. By use of general anesthesia with isoflurane, each dog was positioned in dorsal recumbency and the ventral portion of the abdomen was aseptically prepared for surgery. A midline abdominal incision was made to perform nephrectomy, remove parasites free within the abdominal cavity, or both. The vessels and ureter were identified and ligated with polyglactin 910 and severed. Female dogs were ovariohysterectomized. The abdomen was closed via a 3-layer closure. The linea alba and subcutaneous tissues were closed with polyglactin 910 in a continuous pattern. The skin incision was closed with simple interrupted sutures of size 2–0 monofilament nylon. Male dogs were castrated through a prescrotal incision. Ten dogs received ceftriaxone (30 mg/kg [13.6 mg/lb], IV) immediately before surgery and cephalexin (30 mg/kg, PO, q 24 h) for 5 to 10 days after surgery. Five dogs received doxycycline (10 mg/kg [4.5 mg/lb], PO, q 24 h) 5 days before and 25 days after surgery because of suspected Ehrlichia canis infection. Meloxicam (0.1 mg/kg [0.04 mg/lb], IV, q 24 h) was administered immediately before and for 3 days after surgery (PO), and dipyrone (25 mg/kg [11.36 mg/lb], PO, q 12 h) after surgery in all dogs. Tramadol chlorhydrate (4 mg/kg [1.81 mg/lb], SC, q 12 h) was administrated if necessary. Male and female parasites were quantified according to location. The damaged kidney was evaluated grossly through point scores, as follows: normal (0) = normal corticomedullary differentiation and absence of parasites; low level of damage (1) = effacement of the medulla and presence of parasites; medium level of damage (2) = effacement of the medulla, partial effacement of the cortex, and presence of parasites; and severe damage (3) = complete effacement of the cortex and medulla, and kidney completely occupied by parasites. Chlorhexidine acetate solution was used daily for topical application on the wound, and the skin sutures were removed 10 days after surgery. All dogs survived and were returned to their owner.

Statistical analysis—Pearson correlation coefficients were used to evaluate the linear relationships between results of imaging techniques and macroscopic findings in relation to tissue damage to the right kidney. Values of P < 0.05 were considered significant.

Results

Eight dogs had D renale ova detected via urinalysis. In 12 dogs, ultrasonography revealed several ring-like structures with an echogenic wall and anechoic central area in the transverse plane and arrayed as bands in the longitudinal plane in the corticomedullary area the right kidney (Figure 1). Similar structures were observed in the abdominal cavities of 10 dogs (Figure 2).

Figure 1—
Figure 1—

Representative ultrasonographic image (A), CT image (B), and photograph (C) of the right kidney of dogs infested with giant kidney worms (D renale). A—Ultrasonographic image of the right kidney of a dog. Notice several ring-like structures (parasites) with an echogenic wall and anechoic central area in the transverse plane and band-like structures (parasites) in the longitudinal plane. Internal scale bar = 74.5 mm. Scale on right indicates centimeters. B—Computed tomographic image of the right kidney of a dog. Notice loss of corticomedullary differentiation, with discrete uptake of contrast material in the kidney periphery, and several ring-like or elongated structures (parasites) with hyperdense walls and hypodense centers. C—Photograph of the right kidney of a dog. The kidney has been partially incised, revealing numerous parasites.

Citation: Journal of the American Veterinary Medical Association 244, 5; 10.2460/javma.244.5.555

Figure 2—
Figure 2—

Representative CT images (A and B), ultrasonographic image (C), and intraoperative photograph (D) of the abdominal cavity of dogs infested with giant kidney worms (D renale). A—Notice ring-like structures (white arrows) with hyperdense walls and hypodense centers (parasites). B—Notice elongated structures (white arrows) with hyperdense walls and hypodense centers (parasites). C—Notice ring-like structures (white arrows) representing parasites. D—Notice free parasites in the abdominal cavity.

Citation: Journal of the American Veterinary Medical Association 244, 5; 10.2460/javma.244.5.555

A CT scan revealed loss of corticomedullary differentiation in the right kidney, with discrete uptake of contrast material in the periphery and several ring-like or elongated structures with a hyperdense wall and hypodense center in 13 dogs (Figure 1). In 11 dogs, the same structures were observed free in the peritoneal cavity, most frequently near the hepatic lobes on the right side (Figure 2). In 1 dog, a parasite was observed exiting the lateral aspect of the right kidney through the capsule.

Surgery revealed that 13 dogs had a severely damaged right kidney that required nephrectomy (Figure 1). One dog did not have parasites in the kidneys, and 1 dog had been previously nephrectomized, but a parasite was observed free in the abdominal cavity. Most of the parasites found in the abdominal cavity of 7 dogs were lodged near the hepatic lobes on the right side (Figure 2). Seven kidneys had only female parasites, 3 kidneys had only male parasites, and 3 kidneys had both male and female parasites. One dog had only female parasites in the abdominal cavity, 3 dogs had only male parasites in the abdominal cavity, and 3 dogs had both male and female parasites in the abdominal cavity. Serosanguineous fluid in the abdominal cavity and omentum was seen in most of the dogs with parasites free in the abdominal cavity. With regard to damage to the right kidney, strong correlation was found between ultrasonography and CT scores (P < 0.001; r = 0.842), and strong correlations were detected between ultrasonography and macroscopic findings (P = 0.003; r = 0.731) and between CT and macroscopic findings (P = 0.018; r = 0.618). Among the 15 dogs, a score of 2 was recorded in 6 dogs via ultrasonography, in 7 dogs via CT, and in 4 dogs via macroscopic examination. A score of 3 was recorded in 6 dogs via ultrasonography, in 5 dogs via CT, and in 8 dogs via macroscopic examination.

Discussion

Imaging techniques, including ultrasonography5,7,9,11,19–21 and MRI,14 have been used as diagnostic tools for detecting D renale. Magnetic resonance imaging was used in the case of a human in whom parasites were identified in the kidney and bladder.14 Ultrasonography of the kidney in dogs has revealed D renale as ring-like structures with a double-layer wall in the transversal plane,5,7,19–21 as in the present case series. On the other hand, in 2 human cases, dioctophymosis was misdiagnosed with CT as a renal tumor. In one case, the kidney was described as solid and avascular,15 and in the other case, the right kidney had a distinct mass that was hypodense in the center and had contrast enhancement in its periphery.16 In the present study, discrete uptake of contrast material was observed in the periphery of the kidney, but the parasites were identified as ring-like structures with a hyperdense wall and hypodense center.

With regard to the presence or absence of parasites in the kidneys, CT detected all (13/13) affected kidneys, and ultrasonography detected all but one (12/13). Thus, these techniques had > 90% sensitivity for parasite detection, regardless of the number of parasites present. Similarly, the sensitivity for detection of parasites in the abdomen was high, but the specificity was poor, with 4 false-positive results with CT and 4 with ultrasonography and 1 false-negative result with ultrasonography. Other wormlike structures, especially intestines, may have confused the interpreter. Therefore, there was better agreement between CT and ultrasonography than between either of these techniques and surgery. Thus, surgery seems to be the gold standard for quantification of infestation, especially for free parasites in the abdomen. Surgery revealed that 8 of 15 dogs had parasites only in the right kidney, 2 had parasites only in the abdomen, and 5 had parasites in both the right kidney and abdomen.

Ultrasonography and CT were also adequate for characterizing the degree of kidney damage caused by the parasites, and the findings were highly correlated with the macroscopic findings. In general, the parasites erode the renal cortex and medulla, leaving only the capsule.1,3,7,17,18 Contrast CT revealed discrete uptake of contrast material in the periphery of the kidney, suggesting that the kidney was nonfunctional. Nephrectomy was necessary in the cases in which parasites were found in the kidney (13 dogs). In addition, adhesions and peritonitis may occur if a parasite is located in the abdominal cavity.1,6,17 In the present study, all dogs in which parasites were present in the abdominal cavity had serosanguineous peritoneal fluid and omental inflammation.

Dioctophyme renale ova were detected in the urine of 8 of the 15 dogs and were associated with female parasites in the right kidney, which was confirmed by macroscopic findings. However, 2 dogs in the present study had female parasites in the right kidney, but ova were not observed in the urine, probably because the female parasites were not gravid.17

In the present study, ultrasonography and CT were effective imaging methods for determining the presence of D renale in the kidney and less effective for detecting free parasites in the abdominal cavity. Care should be taken to avoid misidentifying normal structures as parasites, especially in the abdominal cavity.

a.

MyLab Alpha, Esaote, Genoa, Italy.

b.

Shimadzu SCT-7800CT, Shimadzu Corp, Kyoto, Japan.

References

  • 1. Osborne CA, Stevens JB, Hanlon GF, et al. Dioctophyma renale in a dog. J Am Vet Med Assoc 1969; 155:605620.

  • 2. Kommers GD, Ilha MRS, Barros CSL. Dioctophymosis in dogs: 16 cases. Cienc Rural 1999; 29:517522.

  • 3. Pereira BJ, Girardelli GL, Trivilin LO, et al. The occurrence of dioctophymosis in dogs from Municipality of Cachoeiro do Itapemirim in the State of Espírito Santo, Brazil, from May to December of 2004. Rev Braz Parasitol Vet 2006; 15:123125.

    • Search Google Scholar
    • Export Citation
  • 4. Nakagawa TL, Bracarense A, dos Reis AC, et al. Giant kidney worm (Dioctophyma renale) infections in dogs from Northern Paraná, Brazil. Vet Parasitol 2007; 145:366370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Soler M, Cardoso L, Teixeira M, et al. Imaging diagnosis—Dioctophyma renale in a dog. Vet Radiol Ultrasound 2008; 49:307308.

  • 6. Lemos LS, Santos ASO, Rodrigues ABF, et al. Extrarenal lesion caused by Dioctophyma renale eggs in an erratic cycle in a dog. Int J Morphol 2010; 28:10311034.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Ferreira VL, Medeiros FP, July JR, et al. Dioctophyma renale in a dog: clinical diagnosis and surgical treatment. Vet Parasitol 2010; 168:151155.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Sousa AAR, Sousa AAS, Coelho MCOC, et al. Dioctophymosis in dogs. Acta Sci Vet 2011; 39:14.

  • 9. Cottar BH, Dittrich G, Ferreira AA, et al. Ultrasound findings in dogs with Dioctophyma renale—a retrospective study. Vet Zootec 2012; 19:811.

    • Search Google Scholar
    • Export Citation
  • 10. Mech LD. Spatial and temporal differences in giant kidney worm, Dictophyma renale, prevalence in Minnesota mink, Mustela vison. Can Field Nat 2008; 122:162165.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Ishizaki MN, Imbeloni AA, Muniz JAPC, et al. Dioctophyma renale (Goeze, 1782) in the abdominal cavity of a capuchin monkey (Cebus apella), Brazil. Vet Parasitol 2010; 173:340343.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Verocai GG, Measures LN, Azevedo FD, et al. Dioctophyme renale (Goeze, 1782) in the abdominal cavity of a domestic cat from Brazil. Vet Parasitol 2009; 161:342344.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Tokiwa T, Harunari T, Tanikawa T, et al. Dioctophyme renale (Nematoda: Dioctophymatoidea) in the abdominal cavity of Rattus norvegicus in Japan. Parasitol Int 2011; 60:324326.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Sardjono TW, Purnomo BB, Iskandar A, et al. Dioctophymatosis renalis in humans: first case report from Indonesia, in Proceedings. Assoc Southeast Asian Nations Cong Trop Med Parasitol 2008;9093.

    • Search Google Scholar
    • Export Citation
  • 15. Li G, Liu C, Li F, et al. Fatal bilateral dioctophymatosis. J Parasitol 2010; 96:11521154.

  • 16. Gu Y, Li G, Zhang J, et al. Dioctophyma renale infection masquerading as a malignancy. Kidney Int 2012; 82:1342.

  • 17. Liu D. Dioctophyme. In: Molecular detection of human parasitic pathogens. Boca Raton, Fla: Taylor & Francis, 2012;535538.

  • 18. Alvarenga J, Matera JM, Barros PSM, et al. Dioctophyma renale in a dog. Mod Vet Pract 1984; 65:125.

  • 19. Secchi P, Valle SF, Brun MV, et al. Videolaparoscopic nephrectomy in the treatment of canine dioctophymosis. Acta Sci Vet 2010; 38:8589.

    • Search Google Scholar
    • Export Citation
  • 20. Maia VCC, Vieira SL, Oliveira PC, et al. Dioctofimosis inguinal in dog—case report. Vet Zootec 2012; 19:8688.

  • 21. Veiga CCP, Oliveira PC, Ferreira AMR, et al. Dioctophimosis in pregnant uterus in dog—case report. Braz J Vet Med 2012; 34:188191.

    • Search Google Scholar
    • Export Citation
  • 22. Silveira LL, Lemos LS, Ferreira FS, et al. Comparative analysis among the techniques of sedimentation-centrifugal and fast sedimentation (Paratest) on identification of eggs of Dioctophyma renale in piss of dogs. J Bras Cienc Anim 2009; 2:150158.

    • Search Google Scholar
    • Export Citation
  • Figure 1—

    Representative ultrasonographic image (A), CT image (B), and photograph (C) of the right kidney of dogs infested with giant kidney worms (D renale). A—Ultrasonographic image of the right kidney of a dog. Notice several ring-like structures (parasites) with an echogenic wall and anechoic central area in the transverse plane and band-like structures (parasites) in the longitudinal plane. Internal scale bar = 74.5 mm. Scale on right indicates centimeters. B—Computed tomographic image of the right kidney of a dog. Notice loss of corticomedullary differentiation, with discrete uptake of contrast material in the kidney periphery, and several ring-like or elongated structures (parasites) with hyperdense walls and hypodense centers. C—Photograph of the right kidney of a dog. The kidney has been partially incised, revealing numerous parasites.

  • Figure 2—

    Representative CT images (A and B), ultrasonographic image (C), and intraoperative photograph (D) of the abdominal cavity of dogs infested with giant kidney worms (D renale). A—Notice ring-like structures (white arrows) with hyperdense walls and hypodense centers (parasites). B—Notice elongated structures (white arrows) with hyperdense walls and hypodense centers (parasites). C—Notice ring-like structures (white arrows) representing parasites. D—Notice free parasites in the abdominal cavity.

  • 1. Osborne CA, Stevens JB, Hanlon GF, et al. Dioctophyma renale in a dog. J Am Vet Med Assoc 1969; 155:605620.

  • 2. Kommers GD, Ilha MRS, Barros CSL. Dioctophymosis in dogs: 16 cases. Cienc Rural 1999; 29:517522.

  • 3. Pereira BJ, Girardelli GL, Trivilin LO, et al. The occurrence of dioctophymosis in dogs from Municipality of Cachoeiro do Itapemirim in the State of Espírito Santo, Brazil, from May to December of 2004. Rev Braz Parasitol Vet 2006; 15:123125.

    • Search Google Scholar
    • Export Citation
  • 4. Nakagawa TL, Bracarense A, dos Reis AC, et al. Giant kidney worm (Dioctophyma renale) infections in dogs from Northern Paraná, Brazil. Vet Parasitol 2007; 145:366370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Soler M, Cardoso L, Teixeira M, et al. Imaging diagnosis—Dioctophyma renale in a dog. Vet Radiol Ultrasound 2008; 49:307308.

  • 6. Lemos LS, Santos ASO, Rodrigues ABF, et al. Extrarenal lesion caused by Dioctophyma renale eggs in an erratic cycle in a dog. Int J Morphol 2010; 28:10311034.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Ferreira VL, Medeiros FP, July JR, et al. Dioctophyma renale in a dog: clinical diagnosis and surgical treatment. Vet Parasitol 2010; 168:151155.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Sousa AAR, Sousa AAS, Coelho MCOC, et al. Dioctophymosis in dogs. Acta Sci Vet 2011; 39:14.

  • 9. Cottar BH, Dittrich G, Ferreira AA, et al. Ultrasound findings in dogs with Dioctophyma renale—a retrospective study. Vet Zootec 2012; 19:811.

    • Search Google Scholar
    • Export Citation
  • 10. Mech LD. Spatial and temporal differences in giant kidney worm, Dictophyma renale, prevalence in Minnesota mink, Mustela vison. Can Field Nat 2008; 122:162165.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Ishizaki MN, Imbeloni AA, Muniz JAPC, et al. Dioctophyma renale (Goeze, 1782) in the abdominal cavity of a capuchin monkey (Cebus apella), Brazil. Vet Parasitol 2010; 173:340343.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Verocai GG, Measures LN, Azevedo FD, et al. Dioctophyme renale (Goeze, 1782) in the abdominal cavity of a domestic cat from Brazil. Vet Parasitol 2009; 161:342344.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Tokiwa T, Harunari T, Tanikawa T, et al. Dioctophyme renale (Nematoda: Dioctophymatoidea) in the abdominal cavity of Rattus norvegicus in Japan. Parasitol Int 2011; 60:324326.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Sardjono TW, Purnomo BB, Iskandar A, et al. Dioctophymatosis renalis in humans: first case report from Indonesia, in Proceedings. Assoc Southeast Asian Nations Cong Trop Med Parasitol 2008;9093.

    • Search Google Scholar
    • Export Citation
  • 15. Li G, Liu C, Li F, et al. Fatal bilateral dioctophymatosis. J Parasitol 2010; 96:11521154.

  • 16. Gu Y, Li G, Zhang J, et al. Dioctophyma renale infection masquerading as a malignancy. Kidney Int 2012; 82:1342.

  • 17. Liu D. Dioctophyme. In: Molecular detection of human parasitic pathogens. Boca Raton, Fla: Taylor & Francis, 2012;535538.

  • 18. Alvarenga J, Matera JM, Barros PSM, et al. Dioctophyma renale in a dog. Mod Vet Pract 1984; 65:125.

  • 19. Secchi P, Valle SF, Brun MV, et al. Videolaparoscopic nephrectomy in the treatment of canine dioctophymosis. Acta Sci Vet 2010; 38:8589.

    • Search Google Scholar
    • Export Citation
  • 20. Maia VCC, Vieira SL, Oliveira PC, et al. Dioctofimosis inguinal in dog—case report. Vet Zootec 2012; 19:8688.

  • 21. Veiga CCP, Oliveira PC, Ferreira AMR, et al. Dioctophimosis in pregnant uterus in dog—case report. Braz J Vet Med 2012; 34:188191.

    • Search Google Scholar
    • Export Citation
  • 22. Silveira LL, Lemos LS, Ferreira FS, et al. Comparative analysis among the techniques of sedimentation-centrifugal and fast sedimentation (Paratest) on identification of eggs of Dioctophyma renale in piss of dogs. J Bras Cienc Anim 2009; 2:150158.

    • Search Google Scholar
    • Export Citation

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