Source: PURDUE UNIVERSITY submitted to
PREVENTION OF EQUINE SARCOID
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0229482
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2012
Project End Date
Sep 30, 2013
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
PURDUE UNIVERSITY
(N/A)
WEST LAFAYETTE,IN 47907
Performing Department
Veterinary Clinical Sciences
Non Technical Summary
Equine sarcoids are locally invasive skin tumors and represent the most common tumor in equids worldwide. Sarcoids are classified according to their appearance and behavior, with categories including occult (flat), verrucous (wart-like), nodular, fibroblastic (ulcerated), and malevolent (aggressive). Sarcoids can develop in any location, either as a single tumor or as multiple tumors of different type. Although sarcoid tumors do not spread to other organs, they can significantly impact the function and aesthetics of affected equids based on tumor location, size and frequency. Thus, the value of horses with sarcoids is often dramatically decreased. Sarcoid tumors may cause discomfort and can result in ulceration, infection, and occasionally lameness associated with lesion location. Bovine papillomavirus types 1 and 2 (BPV-1, BPV-2) are necessary for sarcoid development, but can also be found in normal horse skin. Quarter Horses, Arabians and Appaloosas have an increased risk for sarcoid development, suggesting a genetic predisposition. Therefore, genetic markers from Quarter Horses with sarcoid will be compared to Quarter Horses without sarcoid. We expect that horses with sarcoid will be genetically different from horses without sarcoid. If this is true, Quarter Horses with the "sarcoid-susceptible" genes will be used for further studies; if not, Quarter Horses will still be used because of their increased risk of sarcoid development compared to other breeds. The next objective is to develop a BPV virus inoculum that when injected into the skin of a genetically-susceptible horse, causes a sarcoid. This inoculum will be grown in the lab, and then injected in escalating doses into the skin of Quarter Horses without sarcoid but with the susceptible genes (if identified above). The dose of inoculum that causes the longest-lasting, largest sarcoids will be selected for vaccine studies. Next, virus-like particles (VLP) that are similar to natural BPV but are non-infectious due to the absence of viral DNA will be used as a vaccine. This VLP-based vaccine will be tested for prophylactic efficacy in BPV-susceptible horses, following a vaccine safety and immune response trial. Vaccine efficacy will be determined by visual and histopathological examination of cutaneous lesions, as well as lymphocyte response tests. The final objective is to explore preventative strategies for recurrence following surgical removal of sarcoids. We suspect that the presence of BPV DNA in histologically tumor-free surgical margins is associated with risk of recurrence, and that increasing quantity of BPV DNA is associated with an increased risk of recurrence. Therefore, quantitation of BPV DNA in excised tumor margins will be used to determine the BPV type and the predictive value of PCR testing for recurrence. Taken together, this information highlights the need for clarification of how and why sarcoids develop to clearly identify at-risk populations. In addition, development of vaccines that can prevent sarcoids will decrease the incidence and severity of disease, and have important implications for papillomavirus infection in other species.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3113810108020%
3113810104020%
3113810109060%
Goals / Objectives
The long-term goal of the proposed study is to elucidate the pathogenesis of equine sarcoid tumors and to implement effective preventative strategies for bovine papillomavirus (BPV), the etiologic agent of equine sarcoids. This cutaneous neoplasm represents the most common equine tumor, and is associated with the only documented case of natural cross-species papillomavirus infection. Tumors are characterized by locally invasive, transformed fibroblasts that are non-permissive for BPV production. This research proposal has four objectives, the first of which is to determine the basis for an apparent breed predilection. A retrospective analysis of sarcoid-bearing equids will be done to provide descriptive data and is expected to corroborate previous findings that Quarter Horses are most commonly affected. Genetic markers from sarcoid-bearing equids will be compared to nonsarcoid-bearing equids of the same breed. The second objective is to develop a BPV inoculum that will induce sarcoid lesions in susceptible horses. Adaptive immune responses to this experimental challenge virus will be evaluated. It is expected that an inoculum dose will be identified that will induce sarcoid-like lesions as well as humoral immune responses. This virus will then be used to test the efficacy of future prophylactic vaccine candidates. The third objective is to develop virus-like particles (VLP) that are morphologically and antigenically similar to natural BPV, but are non-infectious due to the absence of viral DNA. This VLP-based vaccine will be tested for immunoprophylactic efficacy in BPV-susceptible horses, following a vaccine safety and immunogenicity trial. Vaccine efficacy will be determined by visual and histopathological examination of cutaneous lesions, as well as lymphocyte response tests. We expect the vaccine to protect against sarcoid development in naive, susceptible horses following viral challenge. The final objective is to explore preventative strategies for recurrence following surgical excision of sarcoid tumors. Quantitation of BPV DNA in excised tumor margins will be used to determine the BPV type and the predictive value of PCR for recurrence. It is expected that increased BPV DNA in surgical margins will be positively associated with tumor recurrence.
Project Methods
An extensive retrospective analysis of equids affected by sarcoid will be performed to determine risk factors associated with disease by use of the Veterinary Medical Database. Next, we will determine the equine leukocyte antigen (ELA) haplotype distribution for major histocompatibility complex (MHC) Class I and Class II genes among sarcoid-bearing Quarter Horses and nonsarcoid-bearing Quarter Horses. Serum will be collected from 40 Quarter Horses without sarcoid and 40 age-matched Quarter Horses with sarcoid, selected from the PUVTH record database. The ELA haplotype for both MHC Class I and II genes will be determined by using polymorphic microsatellites and sequencing. Cattle papillomas that contain BPV-1, as determined by PCR and sequencing, will be used to obtain infectious virions. Escalating doses of inoculum will be injected intradermally into nonsarcoid-bearing Quarter Horses with the predominant ELA haplotype identified in sarcoid-bearing horses. In the event that association between haplotype and sarcoid status is not identified, nonsarcoid-bearing Quarter Horses will be used regardless of ELA haplotype. Sarcoid-like lesions will be measured, visually categorized as occult, verrucous, nodular, fibroblastic or malevolent, and then biopsied for histopathological assessment and BPV-1 DNA quantification by real-time PCR. The humoral immune response to these injections will be measured. The inoculum dose that results in visible lesions in the majority of horses and persists for the longest period of time will be selected for future prophylactic vaccine studies. Virus-like particles which resemble natural virions will be generated for use as vaccines. Nonsarcoid-bearing Quarter Horses will be inoculated with escalating doses of VLP, followed by lymphocyte response tests. The VLP dose that results in the most robust humoral immune response will be used for future prophylactic vaccine studies. For assessment of prophylactic use of VLP, a randomized, blinded, controlled study will be performed. Horses with a BPV-susceptible ELA haplotype or Quarter Horses will be used in this trial. Horses will receive the VLP vaccine at a dose determined by neutralizing antibody induction for three injections, followed by intradermal infectious virion challenge. Vaccine efficacy will be determined by visual and histopathological examination of lesions, quantitative viral DNA analysis at virion inoculation sites, and serum neutralizing antibody responses. If humoral immune responses to VLP are weak, the AS04 adjuvant will be tested for its ability to enhance these responses. Finally, to test whether presence of BPV DNA in histologically tumor-free surgical margins of sarcoid tumors is associated with recurrence, margins of sarcoid tumors deemed completely resected by histopathology will be tested for BPV DNA by real-time PCR.

Progress 10/01/12 to 09/30/13

Outputs
Target Audience: Veterinarians and colleagues. Changes/Problems: Termination of project is due to lack of funding opportunities for this program and duplication of project by scientists in Vienna, Austria who are further along in the long-term goal of this program. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? The review of equine sarcoids has been published, and the completed project (above) has been submitted for review. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? A review of equine sarcoid by the P.I. was published in Equine Veterinary Education in 2013. The experiments outlined in the final objective of the Hatch proposal have been completed. Our hypotheses were that the presence of bovine papillomavirus (BPV) DNA in histologically tumor-free surgical margins of sarcoid tumors is associated with risk of recurrence, and that increasing quantity of BPV DNA is associated with increasing risk of recurrence. Based on our findings, these hypotheses have been rejected. Copy numbers of BPV in the bulk tumor or in the margins were not associated with the likelihood of recurrence at the excision site. Sarcoid tumor samples with histologically "tumor-free" margins were obtained from the University of California, Davis (UCD), and Purdue University (PU), and diagnosis was confirmed by one pathologist from PU. The sample size for this study was relatively small given the difficulty in achieving complete tumor resection based on histopathology, and because several samples originally identified from UCD were lost. Therefore, a total of 25 tumors were included in the study, 8 of which were associated with recurrence within one year of excision and 17 that were associated with non-recurrence. For each tumor sample, a 5 μm section of bulk tumor and 5 μm of each tumor margin (1-4 margins per sample) were obtained for PCR analysis. Margin samples were pooled for each tumor sample. DNA extraction was performed using an optimized kit for formalin-fixed, paraffin-embedded tissues. Bulk tumors and tumor margins were tested for the presence of BPV type 1 (BPV-1) and BPV type 2 (BPV-2) DNA by traditional (qualitative) PCR amplification of the E2 gene region. Real-time (quantitative) PCR was done using primers that were complimentary to shared sequences between BPV-1 and BPV-2, and TaqMan® probes that were unique to each BPV type. Serial dilutions of a BPV plasmid were used to generate a standard curve and an equine glyceraldehyde-3-phosphate dehydrogenase (GAPDH) gene primer/probe set was used as an internal control for normalization of input DNA. Data were reported as viral copies/cell and analyzed using a Wilcoxin Rank Sum test. The P-value was set at <0.05. Bovine papillomavirus-1 DNA was found in 100% (n = 25) of FFPE tumor samples and in 84% (n = 21) of samples from histologically "clean" surgical margins. Bovine papillomavirus-2 DNA was found in 8% (n = 2) of tumors, and was not found in any margin sample. Bovine papillomavirus-1 DNA was more likely to be found in tumor and margins compared to BPV-2 (P < 0.001). There was no significant difference in the presence of BPV-1 in the tumor compared to surgical margins (P = 0.11). Although quantitative (real time) PCR was more sensitive in detecting the presence of BPV DNA in surgical margins compared to qualitative PCR, there was no significant difference in the presence of BPV-1 or BPV-2 DNA in margins of tumors that recurred and those that did not recur for either test. Specifically, there was no difference in the amount of BPV-1 DNA in the surgical margins between the tumors that recurred (median 0; range 0 – 0.13) and those that did not recur (median 0.02; range 0 – 5.00) (P = 0.52). However, the amount (copies/cell) of BPV-1 DNA in tumors that recurred was significantly higher (median 0.32; range 0.04 – 13.61) than in those that did not recur (median 2.12; range 0.13 – 29.62) (P = 0.042). Finally, BPV DNA type, location (tumor versus surgical margin), and quantity (copies/cell) were not associated with odds of recurrence (P > 0.90). The ability to predict recurrence of sarcoid tumors would allow aggressive and/or additional treatments in a timely fashion if recurrence was likely, thereby providing a more favorable prognosis since tumors that recur after surgical excision often behave more aggressively and are not well circumscribed. However, our results do not support further investigation of quantifying BPV DNA in surgical margins of sarcoid tumors to predict recurrence. The manuscript has been submitted to the Journal of Equine Veterinary Science (October 2013) and is pending review.

Publications

  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Taylor SD, Haldorson GJ. A review of equine sarcoid. Equine Vet Educ. 2013;25(4):210-216.
  • Type: Journal Articles Status: Submitted Year Published: 2013 Citation: Taylor SD, Toth B, Baseler LJ, Charney VA, Miller MA. Lack of correlation between papillomaviral DNA in surgical margins and recurrence of equine sarcoids. J Eq Vet Sci. Submitted.