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Biomédica 2018;38:13-8 First report of Dioctophyma renale in Colombia

doi: https://doi.org/10.7705/biomedica.v38i4.4042

CASE PRESENTATION

First report of Dioctophyma renale


(Nematoda, Dioctophymatidae) in Colombia
Ángel A. Flórez1, James Russo2, Nelson Uribe3
1
Facultad de Ciencias Exactas, Naturales y Agropecuarias, Programa de Medicina Veterinaria, Laboratorio de

Parasitología, Universidad de Santander, Bucaramanga, Colombia
2
Escuela de Medicina Veterinaria y Zootecnia, Instituto Universitario de la Paz (UNIPAZ), Barrancabermeja,

Colombia
3
Línea de Parasitología Humana y Veterinaria, Grupo de Investigación en Inmunología y Epidemiología

Molecular (GIEM), Facultad de Salud, Universidad Industrial de Santander, Bucaramanga, Colombia

Dioctophymosis is a zoonotic parasitic disease caused by Dioctophyma renale (Goeze, 1782). It is


distributed worldwide and it affects a large number of wild and domestic mammals.
Here we report the first confirmed case of canine dioctophymosis in Colombia. The animal was found
dead in the streets of the municipality of Yondó, Antioquia, and its dead body was taken to the Instituto
Universitario de la Paz (UNIPAZ) to carry out a necropsy.
A parasite worm was found in the right kidney and sent for identification to the Laboratorio de
Parasitología of the Universidad de Santander (UDES). The specimen was identified as a male of D.
renale upon observing the typical oval and transversely elongated bell-shaped bursa copulatrix with a
spicule and no rays. Another important factor to confirm the diagnosis was the anatomical location in
the kidney. This is the first time D. renale is reported in a stray dog in Colombia.
Key words: Dioctophymatoidea; Enoplida infections; case studies; Colombia.
doi: https://doi.org/10.7705/biomedica.v38i4.4042
Primer reporte de Dioctophyma renale (Nematoda, Dioctophymatidae) en Colombia
La dioctofimosis es una enfermedad parasitaria zoonótica causada por Dioctophyma renale (Goeze,
1782), de amplia distribución mundial, que afecta a un gran número de mamíferos silvestres y domésticos.
Se reporta el primer caso de dioctofimosis canina en Colombia. El animal fue encontrado muerto en
las calles del municipio de Yondó, Antioquia. Su cadáver fue llevado al Instituto Universitario de la Paz
(UNIPAZ) donde se practicó la necropsia.
En el riñón derecho se encontró un parásito, el cual fue enviado al Laboratorio de Parasitología de
la Universidad de Santander para su identificación. El espécimen se identificó como un macho de D.
renale por la típica bursa copulatriz oval y alargada transversalmente en forma de campana, sin rayos y
con una espícula. Otro factor importante para confirmar el diagnóstico fue la ubicación anatómica en el
riñón. Se reporta por primera vez la presencia de D. renale en un perro mestizo callejero en Colombia.
Palabras clave: Dioctophymatoidea; infecciones por Enoplida; estudios de casos; Colombia.
doi: https://doi.org/10.7705/biomedica.v38i4.4042

The nematode Dioctophyma renale (Goeze, 1782) world, with the possible exception of Africa and
belongs to the order Enoplida, family Dioctophy- the Australian continent. In America, it has been
matidae (1); it can measure up to 100 cm long and reported in Argentina, Brazil, Canada, the United
1.2 cm in diameter (2,3). It is commonly called giant States, Paraguay and Uruguay (8).
kidney worm and is one of the largest nematodes
which parasitizes vertebrates. Corresponding author:
Ángel A. Flórez, Laboratorio de Parasitología, campus
This nematode has been reported to infect domestic universitario Lagos del Cacique, Universidad de Santander,
carnivorous and wild animals such as dogs, foxes, Bucaramanga, Colombia
minks, coyotes, ferrets, otters, cats, pigs, horses, Teléfono: (577) 651 6500, extensión1395
cattle, and even humans (4-7). The parasitism it angelflorezmvz@hotmail.com
causes has spread throughout many parts of the Received: 24/08/17; accepted: 21/03/18

Author’s contributions:
All authors contributed to the identification of the parasite, the discussion, the literature review and the drafting of the manuscript.

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Flórez ÁA, Russo J, Uribe N Biomédica 2018;38:13-8

In the literature review we carried out for diocto- The ectopic locations of the parasite in the liver,
phymosis in Colombia, we found only one study in stomach, groin region, and mammary gland differ-
a Neotropical otter population (Lontra longicaudis) entiate the clinical presentation, as well as the num-
that reports eggs with characteristics similar to D. ber of parasites in the definitive host (13,16-18).
renale, but no adult parasites were reported (9). The importance of these parasites for public health
Dioctophyma renale is commonly described in resides in their zoonotic potential demonstrated by
dogs. Brazil and Argentina are the countries with the report of several human clinical cases (8,39-43).
the largest number of reported cases in mammals Dioctophymosis is a zoonotic disease in which
(5,10). In Brazil, cases have been reported in humans can be the definitive host, although the
several states, including Rio Grande do Sul (3,11- location of the parasite in the kidney is not the
20). Similarly, the canine dioctophymosis has been most frequent feature, as the peritoneum and the
reported in various regions of Argentina (10,21-26) skin are the most frequent locations in humans
and Uruguay (27,28). (38-42). Risk factors for human infection include a
The life cycle of D. renale is indirect and it may high prevalence of infected canines, a high level of
involve different types of hosts until the parasite surface contamination, the use of rivers as a means
reaches maturity. The dog is defined as the defini- of transportation, recreation and food fishing (fish,
tive host (11,29). The aquatic annelid Lumbriculus frogs, and eels) (10).
variegatus is the specific intermediary host and fish Here we report the first case of D. renale in
from freshwater and Chaunus ictericus (Bufonidae) Colombia detected in the necropsy of a dog found
are considered paratenic hosts (13,29,30). The in the municipality of Yondó, Antioquia, located
not-segmented egg is ingested by the intermediary near the Magdalena river where the dog possibly
host, hatches on the inside and the larva moves consumed food contaminated with the parasite.
to reach the third stage that infects the definitive Our report describes the lesions found in the dog
host or the paratenic host. The definitive hosts are and discusses how it could have been infected with
infected by ingesting the intermediary host or the this important nematode not previously reported in
paratenic host. The third stage larva penetrates the country.
the wall of the stomach or duodenum, and then
Case presentation
it migrates through the liver and peritoneal cavity
until it reaches the kidney, predominantly the right In August, 2015, the body of a dead dog found in
one, but some parasites stay in the peritoneal the streets of the municipality of Yondó (Antioquia)
cavity (8,31-33). However, the parasite has also was taken to the Instituto Universitario de la Paz to
been found in the left kidney, the abdominal cavity, carry out a necropsy. The dog was a male mongrel
the thoracic cavity, the ureters, the bladder and the about 8 years old and its weight was 10 kg. A
subcutaneous tissue of dogs and other definitive parasite was found in its right kidney and was sent
hosts (11,13,34-36). to the Laboratorio de Parasitología of the University
of Santander (UDES) for identification.
Normally the infection in dogs is subclinical (11,34),
but the affected animals can present compressive Materials and methods
atrophy of the parenchyma, dilation of the renal A complete post-mortem examination was per-
pelvis, and ureteral obstruction. The most striking formed for teaching purposes, giving special
lesion is the progressive destruction of the renal attention to the thoracic and abdominal cavities.
parenchyma, which, in the most severe cases, can The parasite was preserved in alcohol and sent to
reach a stage where only a thin capsule contains the Laboratorio de Parasitología at the Universidad
the parasite and hemorrhagic exudate (37,38). de Santander (UDES) in Bucaramanga.
The clinical presentation of dioctophymosis can be To identify the parasite, the morphological charac-
initially asymptomatic because the non-infected teristics of the external genital structures of the
kidney is usually capable of assuming the functions genus, as well as the size and color of the nematode
of the infected one. Individuals typically present and its anatomical location, were taken into consi-
symptoms including renal colic, hematuria, and deration (44,45). A definitive taxonomic key for the
pyuria. If the parasite migrates to the ureter and the identification of this species is the presence in males
urethra, it blocks the flow of urine, which can lead of a bell-shaped copulatory bursa with no rays and
to death by uremia and anuria. a spicule measuring 0.5 to 0.6 cm long (46).

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Biomédica 2018;38:13-8 First report of Dioctophyma renale in Colombia

Discussion
The macroscopic features observed at the necropsy,
such as the location of the parasite in the kidney
and its red color, led to the identification of D. renale
in almost a definitive way because of its large size,
which makes this procedure an important diagnosis
method. The final identification of the parasite as
a male of D. renale was based on its morphologi-
cal characteristics, mainly the typical bell-shaped
bursa copulatrix with no rays and a protruding
spicule of 0.5 to 0.6 cm in length (3,30,35,47,48),
which are characteristic of this species (figure 1).
The nematode measured 17 cm in length and 3
mm in diameter (figure 2). During the necropsy, no Figure 1. The large bell-shaped copulatrix bursa with a spicule
significant macroscopic lesions were observed. that protrudes and no rays, characteristic of Dioctophyma renale

In the literature review we carried out on diocto-


phymosis in Colombia, we found only one study
in a Neotropical otter population (L. longicaudis).
Only eggs with characteristics similar to D. renale
were reported, so there was no certainty about
the presence of adult parasites or about eggs
effectively corresponding to the parasite (9).
The dead body of the dog did not present signifi-
cant lesions, and it did not show signs that it had
been hit by a car either. The parenchyma of the
right kidney was completely destroyed and only the
organ capsule was left (figure 3). Figure 2. The parasite measured 17 cm in length and 3 mm in
diameter; a reddish coloration was observed.
In the necropsy, a male specimen of D. renale
was found in the right kidney of the animal. This
anatomical location of the specimen coincided
with the majority of reports of this parasite
(3,11,12,27,37,49-51) and is related to the anatom-
ical position of this organ in front of the duodenum,
where D. renale frequently leaves the intestine
during its migratory route (52). The location of
the parasite in the left kidney is less frequent,
as it occurs when it crosses the stomach in the
greater curvature or develops a cyst around the
liver associated with its migration through the lower
curvature of the stomach (11).
In a retrospective study of 16 cases of D. renale
infection in dogs, all diagnoses were based on
necropsy findings (11). In most of the cases, the
Figure 3. Parenchyma of the right kidney completely destroyed
parasitic infection by D. renale in these animals by the parasite after eating the insides of the kidney leaving only
was found during the necropsy. Clinical diagnosis the renal capsule of the organ
is difficult given that signs and symptoms have no
specificity and many individuals are asymptomatic
of the abdominal cavity (38). In addition, in cases
(11,34,37,38,53).
where there is a loss of renal parenchyma with
In some cases, canine dioctophymosis can be concomitant hypertrophy of the non-parasitized
diagnosed by parasitological examination of the kidney, the diagnosis can be done by performing
urine (34,35), or during an exploratory laparotomy an ultrasound (Oliveira LL, Attallah FA, Santos CL,

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Flórez ÁA, Russo J, Uribe N Biomédica 2018;38:13-8

Wakofs TN, Rodrigues MC, Santos AE. O uso da Santander (UIS) and to Professor Jesús Antonio
ultrassonografia para o diagnóstico de Dioctophyma Betancourt-Echeverri for his support on identifying
renale em ca˜o–relato de caso. In: Annals V Con- the parasite under study.
ferência Sul-americana de Medicina Veterinária.
Conflicts of interest
Rio de Janeiro, Brazil, 2005) or a radiograph (54).
None to declare
In the case we report, only one adult parasite was
found in the dog’s right kidney. However, an unu- Funding
sual case of canine dioctophymosis was reported
Universidad de Santander (UDES)
in Brazil, in which 28 worms of both sexes were
found in the abdominal cavity of a 2-year-old male References
canine, and a single parasite in the right kidney (3). 1. Barriga O. Las enfermedades parasitarias de los anima-
This may be the case with the largest number of les domésticos en la América Latina. Santiago: Editorial
specimens of D. renale in dogs ever reported. Germinal; 2002. p. 247.
2. Kumar V, Vercruysse J, Vandesteene R. Studies on two
The dog in our report was found in the streets of the cases of Dioctophyma renale (Goeze, 1782) infection in
municipality of Yondó (Antioquia), with access to the Chrysocyon brachyurus (Illiger). Acta Zool Pathol Antverp.
Magdalena River. It is very likely that this dog spent 1972;56:83-98.
all its life living on the streets, feeding of garbage 3. Monteiro SG, Sallis LS, Stainki DR. Infecção natural por
and discarded food. Taking into account these risk trinta e quatro helmintos da espécie Dioctophyma renale
factors, it may have ingested the intermediate host (Goeze, 1782) em um cão. Revista da Faculdade de
or the paratenic host of D. renale. This is consistent Zootecnia, Veterinária e Agronomia. 2002;9:95-9.
with other reports by different authors in which 4. Correa O, Bauer A. Dioctofimose canina. Rev Fac Agron
canine dioctophymosis was found predominantly Vet UFRGS. 1967;5:37-41.
in stray dogs (11,13,34) and it may suggest that 5. Amato JF, Grisi L, Rosa VL. Reunião dos casos brasileiros
stray dogs are more susceptible to the infection, but de dioctofimose canina, com registro de mais alta
intensidade de infecção por Dioctophyma renale (Goeze,
the definitive condition is associated with the type
1782). Revista Brasilera Biologica. 1976;36:117-22.
of food that such dogs eat, unlike purebred dogs
or domestic pets that normally remain indoors and 6. Mech LD, Tracy ST. Prevalence of giant kidney worm
(Dioctophyma renale) in wild mink (Mustela vison) in
are fed with a healthy and balanced diet (11,13). In Minnesota. Am Midl Nat. 2001;145:206-9. https://doi.org/10.
a report from southern Brazil, a stray dog was fed 1674/0003-0031(2001)145[0206:POGKWD]2.0.CO;2
with fish and its viscera, which was considered the 7. Taylor MA, Coop RL, Wall RL. Veterinary Parasitology.
main source for the infection (3). Third edition. Ames, Iowa: Blackwell Publishing; 2007. p.
430-1.
This first case of D. renale in a stray dog in Colom-
bia indicates that the parasite may complete its 8. Acha PN, Szyfres B. Zoonosis y enfermedades transmi-
sibles comunes al hombre y los animales. Third edition.
biological cycle in the local conditions of the place Washington, D.C.: Organización Panamericana de la Salud;
where it was found and that, therefore, it could be 2003. p. 806-9.
circulating in this region. Thus, it is necessary to
9. Jaramillo L, Arias L, Soler Tovar D. Helmintos en heces
carry out epidemiological studies in the area to de una población de nutria neotropical (Lontra longicaudis)
determine risk factors for the transmission of the de vida libre en el bajo río Sinú, Córdoba, Colombia (tesis).
infection and to investigate whether there are more Bogotá: Universidad de la Salle; 2015. p. 100.
cases of the disease in dogs and even in humans, 10. Burgos L, Acosta R, Domingo FR, Archelli SM, Gamboa
bearing in mind that it is a zoonosis. M, Linzitto OR, et al. Prevalence of a zoonotic parasite,
Dioctophyma renale (Goeze, 1782), among male canines
The present case report proves for the first time the in a wild riverside area of La Plata river, province of Buenos
presence of the nematode D. renale in a canine in Aires, Republic of Argentina. Rev Patol Trop. 2014;43:420-
6. https://doi.org/10.5216/rpt.v43i4.33603
Colombia, which may indicate that in similar environ-
ments it would be possible to find the intermediate 11. Kommers GD, Ilha MR, Barros CL. Dioctofimose em
or paratenic host of this giant kidney worm. cães: 16 casos. Cienc Rural. 1999;29:517-22. https://doi.
org/10.1590/S010384781999000300023
Acknowledgments 12. Satiko KF, Shimada MT, Suzuki SN, Osaki SC, Bruno
C, Vitto RF, et al. Dioctophymosis occurrence in two
We would like to express our deep and sincere dogs in Guarapuava city, Paraná State. Semin Cienc
gratitude to the Laboratorio de Parasitología of Agrar. 2003;24:177-80. https://doi.org/10.5433/1679-0359.
the Facultad de Salud at Universidad Industrial de 2003v24n1p177

16
Biomédica 2018;38:13-8 First report of Dioctophyma renale in Colombia

13. Nakagawa TL, Bracarense AP, Reis AC, Yamamura 29. Pedrassani D. Aspectos morfológicos, imunológicos e epi-
MH, Headley SA. Giant kidney worm (Dioctophyma demiológicos de Dioctophyme renale em cães no distrito
renale) infections in dogs from Northern Paraná, Brazil. de São Cristóvão, Três Barras, Santa Catarina. Tese de
Vet Parasitol. 2007;145:366-70. https://doi.org/10.1016/j. Doutorado em Medicina Veterinária Preventiva. Jaboticabal,
vetpar.2006.10.027 SP.: Faculdade de Ciências Agrárias e Veterinárias,
Universidade Estadual Paulista; 2009. p. 118.
14. Colpo CB, Silva AS, Monteiro SG, Stainki DR, Camargo
DG, Colpo ET. Ocorrência de Dioctophyma renale em cães 30. Alves GC, Silva DT, Neves MF. Dioctophyma renale:
no município de Uruguaiana – RS. Rev FVZA. 2007;14: o parasita gigante do rim. Revista Cientifica Eletrônica
175-80. Medicina Veterinaria. 2007;4:1-6.
15. Pedrassani D, Hoppe EG, Tebaldi JH, Nascimento AA. 31. Woodhead AE. Life history cycle of the giant kidney worm,
Chaunus ictericus (Spix, 1824) as paratenic host of the Dioctophyma renale (Nematoda), of man and many other
giant kidney worm Dioctophyme renale (Goeze, 1782) mammals. Trans Am Microsc Soc. 1950;69:21-46.
(Nematoda: Enoplida) in São Cristóvão district, Três
Barras county, Santa Catarina state, Brazil. Vet Parasitol. 32. Hallberg CW. Dioctophyma renale (Goeze, 1782) a study
2009;165:74-7. https://doi.org/10.1016/j.vetpar.2009.07.017 of the migration routes to the kidneys of mammals and
resultant pathology. Trans Am Microsc Soc. 1953;72:351-63.
16. Lemos LS, Santos ASO, Rodrigues ABF, Goulart MLVS,
Almeida LG, Silveira LS. Extrarenal lesion caused by 33. Bowman D. Georgis Parasitología para veterinarios. Ninth
Dioctophyma renale eggs in an erratic cycle in a dog. Int edition. España: Elsevier; 2011. p. 464.
J Morphol.2010;28:1031-4. https://doi.org/10.4067/S0717-
34. Kano FS, Shimada MT, Suzuki SN, Osaki SC, Menarim
95022010000400008
BC, Ruthes FR, et al. Ocorrência da dioctofimose em
17. Stainki DR, Pedrozo JC, Gaspar LF, Zanette RA, Silva dois cães no município de Guarapuava/PR. Semin Cienc
AS, Monteiro SG. Urethral obstruction by Dioctophyma Agrar. 2003;24:177-80. https://doi.org/10.5433/1679-0359.
renale in puppy. Comp Clin Path. 2011;20:535-7. https://doi. 2003v24n1p177
org/10.1007/s00580-010-1169-0
35. Leite LC, Cirio SM, Diniz JM, Luz E, Navarro-Silva MA,
18. Sousa AA, de Sousa AA, Coelho MC, Quessada AM, de Silva AW, et al. Lesões anatomopatológicas presentes
Freitas MV, Moraes RF. Dioctophymosis in dogs. Acta Sci na infecção por Dioctophyma renale (Goeze, 1782)
Vet. 2011;39:985. em cães domésticos (Canis familiaris Linnaeus, 1758).
Archives of Veterinary Science. 2005;10:95-101. https://doi.
19. Silveira CS, Diefenbach A, Mistieri ML, Machado IR,
org/10.5380/avs.v10i1.4091
Anjos BL. Dioctophyma renale em 28 cães: aspectos
clinicopatológicos e ultrassonográficos. Pesqui Vet Bras. 36. Verocai GG, Measures LN, Azevedo FD, Correia TR,
2015;35:899-905. https://doi.org/10.1590/S0100-736X201 Fernandes JI, Scott FB. Dioctophyma renale (Goeze,
5001100005 1782) in the abdominal cavity of a domestic cat from Brazil.
Vet Parasitol. 2009;161:342-4. https://doi.org/10.1016/j.
20. Silva RJ, Siqueira MC, Carra PS, Müller G, Borelli GF,
vetpar.2009.01.032
Cerqueira SL, et al. Dioctophyme renale (Nematoda: Enal.
oplida) in domestic dogs and cats in the extreme south of 37. Soulsby EJ. Helminths, arthropods and protozoa of
Brazil. Braz J Vet Parasitol Jaboticabal. 2017;26:119-21. domestic animals. Sixth edition. London: Baillière, Tindall &
https://doi.org/10.1590/s1984-29612016072 Cassell; 1978. p. 326-7.
21. Niño SL. Nueva observación de D. renale en perros de 38. Maxie MG. The kidney. In: Jubb KV, Kennedy PC, Palmer
Buenos Aires. Rev Med Vet Parasit.1948;7:1-4. N. The Pathology of Domestic Animals. Fourth edition. San
22. Ortega CF. Dioctofimosis canina: descripción de un caso Diego: Academic Press; 1993. p. 447-538.
clínico. Analecta Vet. 1969;1:45-51. 39. Beaver PC, Khamboonruang C. Dioctophyma-like larval
23. Morini E, Grillo Torrado C. Pluriparasitismo abdominal en nematode in a subcutaneous nodule from man in Northern
perro por D. renale. Asociación de Veterinarios Españoles Thailand. Am J Trop Med Hyg. 1984;33:1032-4. https://doi.
Especialistas en Pequeños Animales.1978;1:6-9. org/10.4269/ajtmh.1984.33.1032

24. Acosta WG, Burgos L, Radman NE. Evaluación de 40. Vibe PP. Dioctophyma infection in humans. Med Parazitol
la presencia renal y extrarrenal de Dioctophyma renale (Mosk).1985;1:83-4.
por ultrasonografia, en caninos y humanos de un área 41. Sun T, Turnbull A, Lieberman PH, Sternberg SS. Giant
endémica. Reie. 2008;3:40. kidney worm (Dioctophyma renale) infection mimicking retro-
25. Meyer SN, Rosso M, Maza YE. Hallazgo de Dioctophyma peritoneal neoplasm. Am J Surg Pathol. 1986;10:508-12.
renale en la cavidad torácica de un canino. Rev Vet. 42. Urano Z, Hadçsegawa H, Katsumata T, Toriyam K, Aoki
2013;24:63-5. Y. Dioctophymatid nematode larva found from human skin
26. Ruiz MF, Zimmermann RN, Aguirre FO, Stassi A, Forti with creeping eruption. J Parasitol. 2001;87:462-5. https://
MS. Dioctofimosis: presentación de un caso clínico. Revista doi.org/10.1645/0022-3395(2001)087[0462:DNLFFH]2.0.
Veterinaria Argentina.2014;31:315. CO;2

27. Bellini E, Ferreira C. Dioctophyma renale en el perro. 43. Ignjatovic I, Stojkovic I, Kutlesic C, Tasic S. Infestation
Primer hallazgo en Uruguay. Veterinaria. 2001;36:21-4. of the human kidney with Dioctophyma renale. Urol Int.
2003;70:70-3. https://doi.org/10.1159/000067695
28. Hernández Z, Supparo E, dos Santos C, Nan F.
Dioctophyma renale en caninos (Canis familiaris) de 44. Lapage G. Parasitología Veterinaria. México, D.F.: Ed.
Uruguay. Neotrop Helminthol. 2014;8:123-30. Continental SA; 1979. p. 642.

17
Flórez ÁA, Russo J, Uribe N Biomédica 2018;38:13-8

45. Soulsby EJ. Parasitología y enfermedades parasitarias en 50. Freitas MG. Helmintología veterinaria. Fourth edition. Belo
los animales domésticos. Seventh edition. México: Inter- Horizonte: Editora Rabelo & Brasil Ltda.; 1977. p. 267-70.
americana; 1987. p. 823.
51. Ferreira VL, Medeiros FP, July JR, Raso TF. Dioctophyma
46. Barriga O. Dioctophymosis. En: Schultz MG, editor. Hand- renale in a dog: clinical diagnosis and surgical treatment.
book series in zoonoses. Boca Ratón: CRC; 1982. p. 83-92. Vet Parasitol. 2010;168:151-5. https://doi.org/:10.1016/j.
47. Anderson RC. Nematode parasites of vertebrates: Their vetpar.2009.10.013
development and transmission. Second edition. Oxon, UK; 52. Olsen OW. Parasitología Animal. Barcelona: Editora AEDOS;
CABI Publishing; 2000. p. 650. 1977. p. 715-9.
48. Measures LN. Dioctophymatosis. In: Samuel WM, Pybus
53. Osborne CA, Stevens JB, Hanlon GF. Dioctophyma renale
MJ, Kocan A, editors. Parasitic diseases of wild mammals.
in a dog. J Am Vet Med Assoc. 1969;155:605-20.
Second edition. Iowa: University Press; 2001. p. 357-64.
https://doi.org/10.1002/9780470377000 54. Brun MV, Beck CA, Mariano MB, Antunes R, Pigatto
49. Silveira CS, Diefenbach A, Mistieri ML, Machado IR, JA. Nefrectomia laparoscópica em cão parasitado por
Anjos BL. Dioctophyma renale em 28 cães: aspectos Dioctophyma renale - Relato de Caso. Arq Ciê Vet Zool
clinicopatológicos e ultrassonográficos. Pesqui Vet Bras. UNIPAR. 2002;5:145-52. https://doi.org/10.25110/arqvet.
2015;35:899-905. https://doi.org/10.1590/S0100-736X2015 v5i1.2002.758
001100005

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