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Neotropical Helminthology
Neotropical Helminthology, 2025, vol. 19 (1), 149-156
RESEARCH NOTE / NOTA CIENTÍFICA
CANINE MULTICENTRIC LYMPHOMA-DERIVED
TRICHURIS VULPIS
HYPERINFECTION
HIPERINFECCIÓN POR
TRICHURIS VULPIS
DERIVADA DEL LINFOMA
MULTICÉNTRICO CANINO
HIPERINFECÇÃO POR
TRICHURIS VULPIS
DERIVADA DE LINFOMA
MULTICÊNTRICO CANINO
David F. Conga
1
*,
Carlos S. Silva
2
,
Geisy C. Oliveira
2
, Samara C. Loura
2
, Liana F. Vasconcelos
2
,
Adriana C. Cardoso
2
& Washington A. Pereira
2
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20251911974
Universidad Nacional
Federico Villarreal
Volume 19, Number 1 (jan - jun) 2025
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
Trichuris vulpis
(Roederer, 1761) is a geohelminth in the large intestine of wild carnivores, including domestic cats and
occasionally humans. However, canine lymphoma, one of the most aggressive neoplasms in the small animal clinic,
tends as a direct consequence of the loss of immunological response. Moreover, such parasite-related infections could
develop into more serious conditions. In this study, we report a
T. vulpis
hyperinfection case in a canine af ected by
multicentric lymphoma. Physical examinations revealed lymphadenomegaly, haematochezia, and hind limb oedema.
Despite the obtained treatment, the patient died. Macroscopic and microscopic examinations revealed congested
lungs and legs, splenomegaly, lymphadenomegaly with leukocyte inf ltration, and bloody large intestine mucosa in
528 adult
T. vulpis
specimens. Periodic coproparasitological examinations and specif c antiparasitic drug applications
1
Grupo de Medicina da Conservação e Saúde Única, Instituto de Desenvolvimento Sustentável Mamirauá (IDSM). Estrada
do Bexiga, 2584-Tefé, Amazonas. CEP: 69553-225.
2
Laboratório de Patologia Animal, Instituto da Saúde e Produção Animal (ISPA), Universidade Federal Rural da Amazônia
(UFRA). Caixa postal, 917. CEP 66.077-530. Belém-Pará - Brazil.
* Corresponding author:
david.conga@mamiraua.org.br
David F. Conga:
https://orcid.org/0000-0003-2891-6531
Carlos S. Silva:
https://orcid.org/0009-0004-3231-380X
Geisy C. Oliveira:
https://orcid.org/0009-0008-0917-8338
Samara C. Loura:
https://orcid.org/0009-0008-3103-8286
Liana F. Vasconcelos:
https://orcid.org/0000-0002-0058-6457
Adriana C. Cardoso:
https://orcid.org/0000-0002-9987-161X
Washington A. Pereira:
https://orcid.org/0000-0001-7140-8124
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Conga
et al
are considered important, beyond preventive examinations for neoplasias, mainly in vulnerable patients such as older
dogs.
Keywords:
Canine lymphoma – hyper-infection – Trichocephalus – Trichuria
RESUMEN
Trichuris vulpis
(Roederer, 1761) es un geohelminto del intestino grueso de los carnívoros silvestres, incluidos los gatos
domésticos y ocasionalmente los humanos. Sin embargo, el linfoma canino, una de las neoplasias más agresivas en
la clínica de pequeños animales, tiende a ser una consecuencia directa de la pérdida de la respuesta inmunológica.
Además, estas infecciones parasitarias podrían derivar en afecciones más graves. En este estudio, informamos de un
caso de hiperinfección por
T. vulpis
en un canino afectado por linfoma multicéntrico. Los exámenes físicos revelaron
linfadenomegalia, hematoquecia y edema de las extremidades traseras. A pesar del tratamiento recibido el paciente
falleció. Los exámenes macroscópicos y microscópicos revelaron pulmones y piernas congestionados, esplenomegalia,
linfadenomegalia con infltración de leucocitos y mucosa del intestino grueso sanguinolenta con 528 especímenes de
T. vulpis
adultos. Se consideran importantes los exámenes coproparasitológicos periódicos y la aplicación de fármacos
antiparasitarios específcos, más allá de los exámenes preventivos de neoplasias, principalmente en pacientes vulnerables
como los perros mayores.
Palabras clave
: hiperinfección – Linfoma canino – Tricuriasis – Tricocefalia
RESUMO
Trichuris vulpis
(
Roederer, 1761)
é um geohelminto do intestino grosso de carnívoros selvagens, incluindo gatos
domésticos e ocasionalmente humanos. De outro lado, o linfoma canino, uma das neoplasias mais agressivas na clínica de
pequenos animais, com uma consequência direta na perda da resposta imunológica. Esta condição tumoral relacionada
ao parasitismo pode evoluir para condições mais graves. Neste estudo, relatamos um caso de hiperinfecção por
T. vulpis
em um canino afetado por linfoma multicêntrico. Os exames físicos revelaram linfadenomegalia, hematoquezia e edema
de membros posteriores. Apesar do tratamento aplicado, o paciente morreu. Os exames macroscópicos e microscópicos
revelaram pulmões e pernas congestionados, esplenomegalia, linfadenomegalia com infltração de leucócitos e mucosa
do intestino grosso sanguinolenta com a observação de 528 espécimes adultos de
T. vulpis
. Exames coproparasitológicos
periódicos e aplicações de medicamentos antiparasitários específcos são considerados importantes, além de exames
preventivos para neoplasias, principalmente em pacientes vulneráveis, como cães idosos.
Palavras-chave:
hiperinfecção –
Linfoma canino – Trichocephalus –Trichuriasis
Canine lymphoma-derived
Trichuris vulpis
hyperinfection
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INTRODUCTION
Canine lymphoma is among the most aggressive
neoplasms in the clinic of small animals with a direct
consequence of losing the immunological response for
afecting the cells of the lymphatic system (Bally
et al
.,
2018) being responsible for immunity and defence.
Te pathological alterations of this neoplasm could
be divided into multicentric, gastrointestinal, and
mediastinal lymphoma, causing lymphadenomegaly,
weight loss, lethargy, vomiting, diarrhoea, respiratory
difculty, and limb oedema (Fighera
et al
., 2020;
Beraldo
et al
., 2020). Helminthic infection cases or
patients with lymphoma are susceptible to an accelerated
parasite load increase, allowing for the proliferation of
infective adult forms as observed in the case of feline
infections by
Aelurostrongylus abstrusus
(Railliet, 1898)
and
Platynosomum illiciens
(Braun, 1901) associated
with lymphoma (Riveros-Pinilla
et al.,
2011: Terra
et al.,
2015).
Trichuris vulpis
Roederer, 1761 is a geohelminth
with macroscopically diferent morphological
characteristics compared to other helminths (Ferraz
et
al
., 2020). Te anterior end of the animal is long and
thin while the posterior part is wider and more robust. It
lays mucilaginous bitamponate eggs, easily recognizable
in laboratory diagnosis. Tis nematode infecting the
large intestine of wild carnivores including domestic
dogs and cats, opportunely afecting humans (Dunn
et
al
., 2002: Areekul
et al
., 2010; Yevstafeva
et al.,
2019).
In most cases, the infection is mild with no considerable
clinical signs. However, in the case of intense infections,
it could cause abdominal pain, rectal prolapse, bloody
diarrhoea, dehydration, anaemia, and progressive weight
loss (Acha & Szyfres, 2005). In this study, we report a
T.
vulpis
hyperinfection case in a canine patient diagnosed
with multicentric lymphoma.
CASE PRESENTATION
In March 2023, a 13-year-old female canine of an
undefned breed was treated at the Veterinary Hospital
of the
Universidade Federal Rural da Amazônia
(1° 27’
31” S 48° 26’ 04.5” O) in the city of Belém-Pará, Brazil.
Te guardian provided the information that the patient
has had progressive weight loss for four months coupled
with a loss of appetite, and that he has previously taken
antiparasitic medication without informing any name.
Te physical examination revealed lymphadenomegaly
in the submandibular, popliteal, inguinal, and
mammary lymph nodes as well as alopecia in the
abdomen, in addition to a slight degree of dehydration,
haematochezia, and oedema in the posterior limbs
with difculties in walking and alterations in cardiac
auscultation. Terefore, we applied furosemide- and
prednisolone-based treatment for oedema and requested
hemocytometry, biochemistry, and oncological cytology
of the lymph nodes.
In the blood count, we observed macrocytic anaemia with
mild hypochromia and thrombocytopenia (160,000 mil/
mm
3
). Te biochemical examination revealed an increased
alkaline phosphatase level of 386.6 U/L (ref: 20–150
U/L). Despite the palliative treatment, the patient died 48
hours after the consultation and underwent an autopsy at
the UFRA Pathology Laboratory. All procediments were
consented by the animal owner.
In the necroscopic examination, the animal displayed
a grade 3 body condition, pale ocular and buccal
conjunctiva, congested lungs and liver with haemorrhagic
areas, splenomegaly with multiple whitish nodules on
the surface, kidneys with dilation of the renal pelvis, and
lymphadenopathy of the submandibular lymph nodes
pre-scapular, axillary, inguinal and popliteal. In the large
intestine, we observed bloody mucosa and the presence
of numerous adult helminths in the colon, rectum, and
anal mucosa. Te lymph node and intestine samples
were cleaved and processed for haematoxylin and eosin
staining and histopathological diagnosis.
Our histopathological analysis unravelled alveolar oedema,
dilated vessels in the liver, and the diagnosis of lymphoma
in the spleen and lymph nodes. Histologically, these
organs exhibited neoplastic lymphocyte cell proliferation
with anisocytosis and an increase in lymphoblasts,
distributed throughout the lymph node tissue, making
cortico-medullary limit observation impossible with no
perception of medullary cords and sinuses. Furthermore,
we observed neoplastic lymphocyte infltrations in the
capsule and perilymph node fat as well as in the blood
and lymphatic vessels.
In the mucosa of the large intestine, we detected
helminthic forms in small cysts. Te epithelial segments
displayed no evidence of any infammatory reaction. In
a second section helminthic forms, including eggs, were
immersed in the mucosa in the autolytic maceration area
(Figures 1B, and C). Nevertheless, we detected capillaries
distended by blood (congestion +) on the liver. Te
hepatocytes contained brown microgranular pigment
(i.e., a lipofuscin characteristic), considering the age of
the patient.
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et al
Figure 1.
Trichuris vulpis
hyperinfection: A) Numerous adult specimens in the bloody mucosa of the
large intestine (arrows). B-C) Two adults segments in large intestine from histopathological section of the
mucosa (arrows). D) anterior end of adult female showing cuticular processes (p), scale bar=500 µm. E)
Vulvar opening in the middle region of the body (v) and uterus flled with eggs (u), scale bar=500 µm. F)
detail of eggs inside the uterus, scale bar=100 µm.
Canine lymphoma-derived
Trichuris vulpis
hyperinfection
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Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
In total, we recovered 528 adult nematodes from the
large intestine (Figure 1A). Tese nematodes exhibited
an elongated and fliform anterior end with the presence
of stichocytes in the oesophagus and a shorter and
thickened posterior part (Figure 1D). Morphologically,
the males displayed a folded or curved posterior with
spikes in the proximal part and a smooth surface in the
distal part, containing a spicule in the male specimens,
while the posterior region of the females had a nearly
straight end of the tail, also containing a vulvar area
(Figure 1E), uterus, and eggs in the internal region of
the body (Figure 1F). Morphometrically, we analysed
20 eggs with an average length and width of 72.11
and 36.57 µm, respectively. Te morphological and
morphometric data were compatible with those of the
species
T. vulpis
.
DISCUSSION
Te most common parasitic helminth infections in
dogs are those caused by
Toxocara canis
(Werner 1782),
Ancylostoma caninum
(Ercolani, 1859
)
, and
T. vulpis
resulting in haematological changes such as anaemia,
eosinophilia, leucocytosis, and lymphocytosis (Dracz
et
al
., 2014). Te clinical signs and anatomopathological
fndings of this case demonstrate a multicentric
lymphoma, weakening the immune system and worsening
parasitic infectious conditions (Vail
et al.
, 2007; Ribeiro
et al
., 2017), resulting in a hyperinfection of adult
nematodes in the large intestine. Te morphological and
morphometric characteristics of the nematodes and eggs
were compatible with those of the species
T. vulpis
(Kagei
et al
., 1986). Tis infection in domestic dogs is common
in peri-urban and rural areas, indicating a prevalence of
over 40% and infections of up to 181 specimens per host
in previous records (Ramos
et al
., 2015).
Te patient, in this case, was presented with hypochromic
anaemia and mild thrombocytopenia, which could be
caused by tumour cell invasion into the bone marrow
or immune-mediated platelet destruction, resulting
from lymphoma. However,
T. vulpis
infection could
have contributed to the blood loss (Ettinger
et al
., 2003;
Bergman
et al
., 2007). Oedema in the limbs of the
patient was a consequence of lymphadenopathy-related
lymphatic fow obstruction (Cardoso
et al
., 2004).
T.
vulpis
infection could have participated to the electrolyte
and haematological imbalance (Venco
et al
., 2011), as
adult
T. vulpis
nematodes secrete enzymes with cytolytic
and haemolytic activities (Kikuchi
&
Okuyama, 1964;
Kirkova
et al
., 2005), beyond bacterial invasion through
the epithelium of the large intestine (Schachter
et al
.,
2020).
Haematological changes (e.g., eosinophilia and anaemia)
and gastrointestinal pathologies (e.g., diarrhoea,
abdominal pain, tenesmus, and rectal prolapse) could
be observed in domestic dogs with trichurosis, mainly
in rural areas with a tropical climate, where the lack of
healthcare for small animals and the soil humidity and
temperature conditions are optimal for the development
of infective larval forms (Unterköfer
et al
., 2022; Borras
et al
., 2023). We highlight that the species
T. vulpis
and
Trichuris suis
Roederer, 1761
present cases of zoonosis
(Areekul
et al
., 2010; Phosuk
et al
., 2018), causing
mild diarrheal gastrointestinal conditions and even
intestinal ulcers in human patients. Terefore, parasitic
agent control and treatment in domestic animals that
accompany humans is important (Dunn
et al
., 2002;
Márquez-Navarro
et al
., 2012; Mohd-Shaharuddin
et
al.,
2019).
Although the type of antiparasitic medication applied
ante mortem by the owner is unknown, this medication
did not exert the expected efect on the patient, either
because it was not specifc to the parasitic agent or due to
underdose. Helminth type-specifc applications and doses
are relevant in the case of serious infections. Moxidectin
and fenbendazole treatment in severe
Strongyloides
stercoralis
Bavay, 1876 infection cases in dogs did not
result in the elimination of adult parasites and larvae,
but the expected efect could be achieved when applying
ivermectin (Unterköfer
et al
., 2022).
In this study, we reported a
T. vulpis
hyperinfection case,
drawing attention by its unusual occurrence. Clinical
severity must be considered in cases when the patient
displays immunodefciency, potentially associated
with neoplastic disease, as in the case of lymphoma. A
routine coproparasitological diagnosis and the periodic
application of specifc antiparasitics for helminth and
protozoan species would be considered important,
especially in vulnerable patients such as older dogs.
ACKNOWLEDGMENTS
CSS and GCO Received scholarship from CNPq
(Conselho Nacional de Desenvolvimento Científco
e Tecnológico). DFC Received scholarship from
Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior (PNPD-CAPES).
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Conga
et al
Author contributions: CRediT (Contributor Roles
Taxonomy)
DFC
= David F. Conga
CSS
= Carlos S. Silva
GCO
= Geisy C. Oliveira
SCL
= Samara C. Loura
LFV
= Liana F. Vasconcelos
ACC
= Adriana C. Cardoso
WAP
= Washington A. Pereira
Conceptualization
: WAP
Data curation
: CSS, GCO, SCL
Formal Analysis:
DFC, CSS, GCO, SCL, LFV, ACC,
WAP
Funding acquisition
: WAP
Investigation
: DFC, CSS, GCO, LFV
Methodology
: LFV, SCL, CSS, GCO
Project administration
: WAP, ACC
Resources
: WAP
Software:
DFC, CSS, GCO, SCL, LFV, ACC, WAP
Supervision
: WAP, ACC
Validation:
DFC, CSS, GCO, SCL, LFV, ACC, WAP
Visualization
: WAP, ACC
Writing – original draft
: DFC, CSS, GCO
Writing – review & editing
: WAP, ACC
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