149 Endoparasites of anurans in the seven cities national park Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025 Neotropical Helminthology Neotropical Helminthology, 2025, vol. 19 (1), 149-156 RESEARCH NOTE / NOTA CIENTÍFICA CANINE MULTICENTRIC LYMPHOMA-DERIVED TRICHURIS VULPIS HYPERINFECTIONHIPERINFECCIÓN POR TRICHURIS VULPIS DERIVADA DEL LINFOMA MULTICÉNTRICO CANINOHIPERINFECÇÃO 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.brDavid F. Conga: https://orcid.org/0000-0003-2891-6531Carlos S. Silva: https://orcid.org/0009-0004-3231-380XGeisy C. Oliveira: https://orcid.org/0009-0008-0917-8338Samara C. Loura: https://orcid.org/0009-0008-3103-8286Liana F. Vasconcelos: https://orcid.org/0000-0002-0058-6457Adriana C. Cardoso: https://orcid.org/0000-0002-9987-161XWashington A. Pereira: https://orcid.org/0000-0001-7140-8124
150 Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025 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 151 Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025 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.
152 Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025 Conga 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 153 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).
154 Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025 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 BIBLIOGRAPHIC REFERENCES Acha P., & Szyfres, B. (2005). Zoonosis y enfermedades transmisibles comunes al hombre. Revista Española de Salud Pública, 79 , 423-423. Areekul, P., Putaporntip, C., Urassaya, P., Prasert, S., & Somchai, J. (2010). Trichuris vulpis and T. trichiura infections among schoolchildren of a rural community in northwestern Tailand: the possible role of dogs in disease transmission. Asian Biomedicin e , 4 , 49-60. Bally, A., Acevedo, K., Pargass, I., Gyan, L., Rajh, S., & Suepaul, R.A. (2020). multicentric TCell lymphoma with a plasmacytoid morphology in a dog. Veterinary Science , 5, 10Beraldo, M.R., Varzim, F.L., & Pulz, L.H. (2020). Linfoma multicêntrico canino: uma sinopse sobre os aspectos clinicopatológicos e alterações laboratoriais. Revista de Educação Continuada em Medicina Veterinária e Zootecnia do CRMV-SP , 18 , 2-3.Bergman, P.J. (2007). Paraneoplasic syndromes. In: Withrow, S.J., Vail, D.M., Withrow & MacEwen’s small animal clinical oncology. W.B. Saunders Company, pp. 77-94. Borras, P., Pérez, M.G., Repetto, S., Barrera, J.P., Risso, M.G., Montoya, A., Miró, G., Fernandez, F., Telesca, L., Britton, C., & Ruybal, P. (2023). First identifcation of Strongyloides stercoralis infection in a pet dog in Argentina, using integrated diagnostic approaches. Parasites & Vectors, 16 , 389. Cardoso, M.J., Machado, L.H., Moutinho, F.Q., & Padovani, C.R. (2004). Linfoma canino achados clínico patológicos. Archives of Veterinary Science, 9 , 25-29. Dracz, R.M., Mozzer, L.R., Fujiwara, R.T., & Santos, L.W. (2014). Parasitological and hematological aspects of co-infection with Angiostrongylus vasorum and Ancylostoma caninum in dogs. Veterinary Parasitology , 200 , 111-116. Dunn, J.J., Columbus, S.T., Aldeen, W.E., Davis, M., & Carroll, K.C. (2002). Trichuris vulpis recovered from a patient with chronic diarrhea and fve dogs. Journal of Clinical Microbiolog y , 40 , 2703-2704. Ettinger, S.N. (2003). Principles of treatment for canine lymphoma. Clinical Techniques in Small Animal Practice, 18 , 92-97.
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156 Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025 Conga et al Yevstafeva, V. А ., Kravchenko, S.O., Gutyj, B.V., Melnychuk, V.V., Kovalenko, P.N., & Volovyk, L.B. (2019). Morphobiological analysis of Trichuris vulpis (Nematoda, Trichuridae), obtained from domestic dogs. Regulatory Mechanisms in Biosystems , 10 , 165-171. Received April 10, 2025.Accepted May 23, 2025.