The route of Besnoitia besnoiti tachyzoites inoculation does not influence the clinical outcome of the infection in calves

Diezma-Díaz, Carlos; Ferre, Ignacio; Re, Michela; Jiménez-Meléndez, Alejandro; Tabanera, Enrique; González-Huecas, Marta; Pizarro-Díaz, Manuel; Yanguas-Pérez, D.; Brum, P.L.; Blanco-Murcia, Javier; Ortega‐Mora, Luis Miguel; Álvarez‐García, Gema

doi:10.1016/j.vetpar.2019.02.001

Cited by 4 publications

(17 citation statements)

References 17 publications

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“…Infected animals developed clinical signs compatible with the acute stage and microscopic lesions characteristic of the chronic stage (Diezma‐Díaz et al, ). In a second trial, 10 6 tachyzoites were inoculated by a subcutaneous and intradermal route to mimic parasite transmission under natural conditions by bloodsucking arthropods and direct contact, with similar results (Diezma‐Díaz et al, ). Accordingly, host (age and inoculation route)‐ and parasite‐dependent factors, such as parasite dose, are not key variables when inducing macroscopic clinical signs of chronic besnoitiosis after cattle inoculation with the tachyzoite stage.…”

Section: Introductionmentioning

confidence: 75%

“…Two recent experimental infections carried out in calves formed the basis for the present work, as identical experimental designs were followed. When tachyzoites were inoculated by intravenous (10 6 , 10 7 and 10 8 tachyzoites) (Diezma‐Díaz et al, ), subcutaneous and intradermal routes (10 6 tachyzoites) (Diezma‐Díaz et al, ), mild to moderate acute besnoitiosis was evident, followed by the absence of the clinical signs and macroscopic lesions characteristic of the chronic phase and scarce intra‐organic distribution of the parasite. The absence of the clinical signs that are characteristic of chronic besnoitiosis hampers the employment of these experimental models based on the inoculation of the tachyzoite stage, regardless of the inoculation route in future drug and vaccines efficacy trials.…”

Section: Discussionmentioning

confidence: 99%

“…We again studied three possible routes of inoculation (intravenous, subcutaneous and intradermal route), which could happen in nature since parasite can be transmitted by bloodsucking arthropods or through lacerations or wounds during direct contact between infected and non‐infected cattle (Álvarez‐García et al, ). The dose of 10 6 bradyzoites was selected according to previous studies done with tachyzoites to compare results obtained with the same parasite dose (Diezma‐Díaz et al, ; Diezma‐Díaz et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…The inoculum consisted of 10 6 bradyzoites (see section 2.3) diluted in 2 ml PBS administered through three different inoculation routes: intravenous inoculation by single jugular venipuncture (G1), subcutaneous inoculation in the left prescapular area (G2) and intradermal inoculation in the thigh area (G3), with the dosage subdivided into ten inoculation points, five of them on each side of the animal and administered with an intradermal Dermojet HR syringe (Akra DermoJet®, Pau, France). The sites of inoculation were the same ones employed in a previous work where tachyzoites were inoculated (Diezma‐Díaz et al, ). Moreover, a non‐infected control group was inoculated with PBS intravenously (G4).…”

Section: Methodsmentioning

confidence: 99%

“…The experimental design, clinical monitoring, samplings (Figure a) and clinical score for the acute (from 1 to 42 days post‐infection) and chronic phase (from 43 to 90 days post‐infection) (Table ) were established in the previous trials (Diezma‐Díaz et al, , ). Fever, lymphadenopathy, cough, nasal and ocular secretion, congestive ocular conjunctiva and general oedema were monitored during the acute phase, along with ocular conjunctival cysts, orchitis and skin lesions during the chronic phase.…”

Section: Methodsmentioning

confidence: 99%

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A model for chronic bovine besnoitiosis: Parasite stage and inoculation route are key factors

Diezma-Díaz

Ferre

et al. 2019

Transbound Emerg Dis

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In this work, an experimental model for chronic besnoitiosis in bovine was developed and characterized. Using a previously established calf model, two new variables (parasite stage and inoculation route) were combined and used. Twelve Holstein Friesian 3‐month‐old male calves were randomly divided into four groups of three animals each. Bradyzoites were obtained from a chronically infected bull and used for inoculation via three different inoculation routes. Three groups were inoculated with 106 bradyzoites by intravenous (G1), subcutaneous (G2) and intradermal (G3) routes, and a non‐infected control group (G4) was inoculated with PBS. The trial lasted for 90 days and included daily clinical monitoring as well as weekly skin biopsies and blood sampling. Sera were obtained to analyse both cellular and humoral responses. Once the calves were euthanized, tissues from the skin, eyes, respiratory and reproductive tracts, among others, were collected to study presence of the parasite. Clinically, the infection was classified as mild to moderate for the acute stage since all infected calves showed lymphadenopathy from four days post‐infection (pi) and fever from one week pi until 24 days pi. However, the most relevant results were achieved during the chronic stage that was classified as moderate to severe. In fact, pathognomonic conjunctival cysts were observed in all infected calves from 40 days pi onwards and were more abundant in G3. Moreover, one calf from this group developed skin lesions (49 days pi). The microscopic tissue cysts and Besnoitia DNA were detected primarily in skin, reproductive tract and respiratory tissue samples, and parasite load was higher in G3. In conclusion, the parasite stage (bradyzoite) and the inoculation route are key factors that influence the outcome of an infection. In particular, the intradermal route led to more severe clinical signs of the chronic phase in the inoculated calves.

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Section: Introductionmentioning

confidence: 75%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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A model for chronic bovine besnoitiosis: Parasite stage and inoculation route are key factors

Diezma-Díaz

Ferre

et al. 2019

Transbound Emerg Dis

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Added value of IgM detection and low avidity index as markers of acute bovine besnoitiosis

Diezma-Díaz

Ferre

Saldias

et al. 2020

Veterinary Parasitology

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Vascular wall injury and inflammation are key pathogenic mechanisms responsible for early testicular degeneration during acute besnoitiosis in bulls

et al. 2020

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Background: Bovine besnoitiosis, caused by the apicomplexan parasite Besnoitia besnoiti, is a chronic and debilitating cattle disease that notably impairs fertility. Acutely infected bulls may develop respiratory signs and orchitis, and sterility has been reported in chronic infections. However, the pathogenesis of acute disease and its impact on reproductive function remain unknown. Methods: Herein, we studied the microscopic lesions as well as parasite presence and load in the testis (pampiniform plexus, testicular parenchyma and scrotal skin) of seven bulls with an acute B. besnoiti infection. Acute infection was confirmed by serological techniques (IgM seropositive results and IgG seronegative results) and subsequent parasite detection by PCR and histological techniques. Results: The most parasitized tissue was the scrotal skin. Moreover, the presence of tachyzoites, as shown by immunohistochemistry, was associated with vasculitis, and three bulls had already developed juvenile tissue cysts. In all animals, severe endothelial injury was evidenced by marked congestion, thrombosis, necrotizing vasculitis and angiogenesis, among others, in the pampiniform plexus, testicular parenchyma and scrotal skin. Vascular lesions coexisted with lesions characteristic of a chronic infection in the majority of bulls: hyperkeratosis, acanthosis and a marked diffuse fibroplasia in the dermis of the scrotum. An intense inflammatory infiltrate was also observed in the testicular parenchyma accompanied by different degrees of germline atrophy in the seminiferous tubules with the disappearance of various strata of germ cells in four bulls. Conclusions: This study confirmed that severe acute besnoitiosis leads to early sterility that might be permanent, which is supported by the severe lesions observed. Consequently, we hypothesized that testicular degeneration might be a consequence of (i) thermoregulation failure induced by vascular lesions in pampiniform plexus and scrotal skin lesions; (ii) severe vascular wall injury induced by the inflammatory response in the testis; and (iii) blood-testis barrier damage and alteration of spermatogenesis by immunoresponse.

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The route of Besnoitia besnoiti tachyzoites inoculation does not influence the clinical outcome of the infection in calves

Cited by 4 publications

References 17 publications

A model for chronic bovine besnoitiosis: Parasite stage and inoculation route are key factors

A model for chronic bovine besnoitiosis: Parasite stage and inoculation route are key factors

Added value of IgM detection and low avidity index as markers of acute bovine besnoitiosis

Vascular wall injury and inflammation are key pathogenic mechanisms responsible for early testicular degeneration during acute besnoitiosis in bulls

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