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Demonstration of Tritrichomonas Foetus in the External Genitalia and of Specific Antibodies in Preputial Secretions of Naturally Infected Bulls

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Demonstration of Tritrichomonas Foetus in the External Genitalia and of Specific Antibodies in Preputial Secretions of Naturally Infected Bulls University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln USDA National Wildlife Research Center - Staff U.S. Department of Agriculture: Animal and Publications Plant Health Inspection Service 1999 Demonstration of Tritrichomonas foetus in the External Genitalia and of Specific Antibodies in Preputial Secretions of Naturally Infected Bulls J. C. Rhyan US Department of Agriculture K. L. Wilson US Department of Agriculture B. Wagner Western College of Veterinary Medicine M. L. Anderson University of California, Davis R. H. Bondurant University of California, Davis See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/icwdm_usdanwrc Part of the Environmental Sciences Commons Rhyan, J. C.; Wilson, K. L.; Wagner, B.; Anderson, M. L.; Bondurant, R. H.; Burgess, D. E.; Mutwiri, G. K.; and Corbeil, L. B., "Demonstration of Tritrichomonas foetus in the External Genitalia and of Specific Antibodies in Preputial Secretions of Naturally Infected Bulls" (1999). USDA National Wildlife Research Center - Staff Publications. 1061. https://digitalcommons.unl.edu/icwdm_usdanwrc/1061 This Article is brought to you for free and open access by the U.S. Department of Agriculture: Animal and Plant Health Inspection Service at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USDA National Wildlife Research Center - Staff Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors J. C. Rhyan, K. L. Wilson, B. Wagner, M. L. Anderson, R. H. Bondurant, D. E. Burgess, G. K. Mutwiri, and L. B. Corbeil This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ icwdm_usdanwrc/1061 Vet Pathol 36:406–411 (1999) Demonstration of Tritrichomonas foetus in the External Genitalia and of Specific Antibodies in Preputial Secretions of Naturally Infected Bulls J. C. RHYAN,K.L.WILSON,B.WAGNER,M.L.ANDERSON,R.H.BONDURANT,D.E.BURGESS, G. K. MUTWIRI, AND L. B. CORBEIL Pathobiology Laboratory, National Veterinary Services Laboratories, US Department of Agriculture, Ames, IA (JCR,1 KLW); Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK, Canada (BW); California Veterinary Diagnostic Laboratory, University of California, Davis, CA (MLA); Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA (RHB); Department of Veterinary Molecular Biology, Montana State University, Bozeman, MT (DEB); and Department of Pathology, Medical Center, University of California, San Diego, CA (GKM,2 LBC) Abstract. Portions of penis and prepuce were collected from 24 bulls with current or recent Tritrichomonas foetus infection. Epididymides were collected from seven of the bulls, and seminal vesicles and prostate were collected from four. Following immunohistochemical staining with two monoclonal antibodies (34.7C4.4 and TF1.15) prepared against T. foetus surface antigens, trichomonads were identified in sections from 15 of the bulls. Organisms were most often located in penile crypts in the midshaft and caudal regions and less often in preputial crypts. Trichomonads were not observed in sections from other genitalia or in subepithelial tissue. T. foetus antigen, however, was present in the cytoplasm of some epithelial cells and the cytoplasm of some mononuclear cells in subepithelial lymphoid aggregates and follicles. Preputial smegma was collected from 16 T. foetus-infected bulls and from 16 control bulls with negative T. foetus cultures. Preputial antibody levels to TF1.17, a surface antigen of T. foetus, were determined by an enzyme-linked immunosorbent assay. Preputial secretions from infected bulls contained specific antibody of each isotype and subisotype tested. IgG1 responses were the greatest, IgM and IgA responses were approximately equal, and IgG2 responses were low. Each isotype and subisotype response in infected bulls was significantly greater than that in the controls. These results confirm previous speculation concerning anatomical sites of infection and suggest that parasite antigen can be taken up and processed locally, resulting in deposition of specific IgG1, IgG2, IgA, and IgM antibodies in the preputial cavity. Key words: Cattle; genitalia; immunity; immunoglobulins; immunohistology; trichomoniasis; Tritrichomo- nas foetus. Bovine trichomoniasis, caused by the protozoa Tri- all regions of the penile and preputial mucosae and trichomonas foetus, is a venereally transmitted infec- occasionally from the urethral orifice.25 Highest num- tion of cattle that produces early pregnancy loss, oc- bers of organisms have been found on the penile mu- casional pyometra, and, less commonly, mid- to late- cosa and adjacent posterior preputial mucosa.18 term abortions. Bulls maintain the infection in the pre- In a previous histopathologic study of naturally and putial cavity and may experience mild transient experimentally infected bulls, no lesions could be spe- balanoposthitis.22 Although young bulls can become cifically attributable to T. foetus infection.25 No organ- infected, infection rates increase with age,13,32 and ev- isms were detected in tissue sections by conventional Ն idence suggests that bulls 4 years of age become stains or fluorescence microscopy using acridine or- 23 persistently infected. T. foetus can be cultured from ange and an immunofluorescent technique that em- ployed a polyclonal antibody against T. foetus. T. foe- 1 Present address: National Wildlife Research Center, Fort tus was considered limited to surface secretions in the Collins, CO. preputial cavity. In heifers and cows, the organism is 2 Present address: Veterinary Infectious Disease Organi- found on the endometrial surface and in endometrial zation, Saskatoon, SK, Canada. glandular lumina.1,26 406 Vet Pathol 36:5, 1999 T. foetus in Bulls 407 Invasion of placental chorion and fetal tissues by T. at 37 C. Sections were then rinsed, and the enzyme activity foetus has been demonstrated using conventional stains was detected using 3% 3-amino-9-ethylcarbozole in N,N-di- and immunohistochemical (IHC) techniques.27,28 Tis- methylformamide (Dako). Sections were counterstained with sue invasion by other species of trichomonads also has Gill II hematoxylin (Surgipath Medical Industries, Grays- been reported,7,31 including prostatic16 and cervical17 lake, IL) for 3 minutes, rinsed in water, and blued in buffer for 1 minute. Coverslips were mounted with an aqueous invasion by Trichomonas vaginalis in human beings. mounting medium (Dako). Nonimmunized rabbit Ig was This variation in the invasiveness of trichomonads substituted for primary antibody as a negative control. A warranted a more detailed study on the location of the commercially available capillary gap system (MicroProbe, organism in the genital tissues of bulls. The bull’s local Fisher Scientific) was used for all IHC staining. immune response to T. foetus infection is poorly un- Preputial smegma was collected for antibody analysis derstood. Systemic immunization of bulls with tricho- from the 14 culture-positive bulls from California plus two monad antigen can prevent or cure infection,11,12 yet more from the same study (16 total). Smegma was also col- unvaccinated bulls often remain persistently infected. lected from 16 control bulls with negative T. foetus cultures. The purposes of this study were to immunohistologi- Positive bulls were cultured many times, but negative bulls cally identify the anatomical sites of T. foetus infection were only cultured once as part of a previously reported 4 in the bull’s genitalia, to determine if T. foetus antigen prevalence study. Because three cultures are recommended to be sure that a bull is negative for T. foetus,3 some of the crosses the epithelium, and to quantify the local (in- negative control bulls may have been false negatives. The trapreputial) antibody responses, by isotype, to the par- samples were collected using a 20-in. dry plastic uterine in- asite. fusion pipette attached to a 12-ml disposable plastic syringe. The pipette was introduced into the preputial cavity up to Materials and Methods the fornix. Several vigorous back and forth movements with Genital tissues from nine bulls from Saskatchewan (Can- simultaneous negative pressure from the syringe were made ada) (bull Nos. 1–9), 14 bulls from California (bull Nos. 10– to collect each sample. The pipette was removed from the 23), and one bull from New Mexico (bull No. 24) were used prepuce and the pipette tip was rinsed in 1 ml of phosphate- in this study. All bulls were beef breeds, and all were from buffered saline (PBS), pH 7.2, or lactated Ringer’s solution. T. foetus-infected herds. Ages of the bulls ranged from 2 to Samples were frozen at Ϫ20 C until used. 6years.AllofthebullsexceptNos.3,5,8,and9were Smegma samples were tested for IgG1, IgG2, IgM, and culture positive for T. foetus at slaughter; Nos. 3, 5, 8, and IgA antibodies to the TF1.17 surface antigen of T. foetus by 9 had been culture positive when tested within 4 months enzyme-linked immunosorbent assay (ELISA) as previously prior to slaughter but were culture negative at slaughter. described21 with modifications. (MAbs TF1.15 and TF1.17 Specimens collected at slaughter included portions of the recognize different epitopes of the same antigen.20)The galea glandis, glans penis, shaft of the penis midway be- TF1.17 antigen was prepared by immunoaffinity purification
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