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BMC Immunology Biomed Central BMC Immunology BioMed Central Research article Open Access Potential effect of prior raccoonpox virus infection in raccoons on vaccinia-based rabies immunization J Jeffrey Root*1, Robert G McLean1, Dennis Slate2, Kathleen A MacCarthy1 and Jorge E Osorio3 Address: 1United States Department of Agriculture, Wildlife Services, National Wildlife Research Center, Fort Collins, CO 80521, USA, 2United States Department of Agriculture, Wildlife Services, National Rabies Management Program, Concord, NH 03301, USA and 3University of Wisconsin – Madison, School of Veterinary Medicine, Madison, WI 53706, USA Email: J Jeffrey Root* - [email protected]; Robert G McLean - [email protected]; Dennis Slate - [email protected]; Kathleen A MacCarthy - [email protected]; Jorge E Osorio - [email protected] * Corresponding author Published: 3 October 2008 Received: 6 September 2007 Accepted: 3 October 2008 BMC Immunology 2008, 9:57 doi:10.1186/1471-2172-9-57 This article is available from: http://www.biomedcentral.com/1471-2172/9/57 © 2008 Root et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The USDA, Wildlife Services cooperative oral rabies vaccination (ORV) program uses a live vaccinia virus-vectored (genus Orthopoxvirus) vaccine, Raboral V-RG® (V-RG), to vaccinate specific wildlife species against rabies virus in several regions of the U.S. Several naturally occurring orthopoxviruses have been found in North America, including one isolated from asymptomatic raccoons (Procyon lotor). The effect of naturally occurring antibodies to orthopoxviruses on successful V-RG vaccination in raccoons is the focus of this study. Results: Overall, raccoons pre-immunized (n = 10) with a recombinant raccoonpox virus vaccine (RCN-F1) responded to vaccination with V-RG with lower rabies virus neutralizing antibody (VNA) titers than those which were not pre-immunized (n = 10) and some failed to seroconvert for rabies VNA to detectable levels. Conclusion: These results suggest that the success of some ORV campaigns may be hindered where raccoonpox virus or possibly other orthopoxvirus antibodies are common in wildlife species targeted for ORV. If these areas are identified, different vaccination strategies may be warranted. Background Several naturally occurring orthopoxviruses can be found Oral rabies vaccination (ORV) programs for raccoons are throughout the world. For example, bank voles (Clethrion- common in the eastern U.S. Raboral V-RG® (V-RG) is the omys glareolus), woodmice (i.e., long-tailed field mice: only licensed oral rabies vaccine for wildlife in the U.S. Apodemus sylvaticus) and Nowray lemmings (Lemmus lem- This vaccine utilizes a live vaccinia virus (genus Orthopox- mus) yielded evidence of orthopoxvirus antibodies in virus) vector. Because oral rabies vaccination rates in rac- Norway [3]. Similar associations were noted for select car- coons (Procyon lotor) can be low in some areas [1], and nivore species in Fennoscandia [4] and red fox (Vulpes vul- large expenses are involved in these types of campaigns pes) in Germany [5]. In the U.S., endemic orthopoxvirus [2], it is important that all key factors that could affect vac- examples include volepox virus found in California voles cination rates be addressed. (Microtus californicus; [6]), raccoonpox virus found in rac- Page 1 of 7 (page number not for citation purposes) BMC Immunology 2008, 9:57 http://www.biomedcentral.com/1471-2172/9/57 coons [7,8], and skunkpox virus found in a striped skunk their antibody titers (1:5) were all at the threshold of (Mephitis mephitis; reviewed by [9]). Additional unrecog- detection (geometric mean titer {GMT} < 1:5; treating all nized orthopoxviruses may exist in the U.S. For raccoon- < 1:5 titers as one significant digit less than the detection pox and skunkpox viruses, it is unknown whether the limit). Assays on a second pre-treatment blood sample species from which these viruses were obtained are the were identical with one exception; the titer of one raccoon true reservoir species (e.g., these viruses, like many other increased from < 1:5 (e.g., below the detection limit) to orthopoxviruses, may be rodent-hosted), as little field 1:5 during its quarantine period prior to experimentation work has been conducted on these viruses since their dis- (GMT < 1:5). Of these animals with pre-existing covery. orthopoxvirus antibodies at low titers, all yielded evi- dence of rabies VNA following their second dose of V-RG. It is unknown whether previous exposure to these North American orthopoxviruses can inhibit the effectiveness of Thirty days after a single dose (DPI) with the RCN-F1 vac- V-RG vaccination in raccoons. However, it has been noted cine (108 pfu), nine of 10 RCN-F1 treated raccoons (treat- that preexisting immunity to vaccinia virus may impede ment) had detectable antibodies to raccoonpox virus (i.e., the replication of vaccinia virus vectors and decrease the ≥1:5; range = < 1:5 – 1:20; GMT = 1:7). At that time, seven response to the recombinant product [10]. The subject of of 10 control raccoons (those only vaccinated with V-RG) preexisting immunity has received some attention for were negative for antibodies reactive with this test; the select vectored vaccines. For example, researchers [11] remaining three animals had pretreatment antibodies indicated that mucosal vaccination overcame the barrier (range < 1:5 – 1:5; GMT = < 1:5). Sixty-nine days following of preexisting orthopoxvirus immunity of mice initially the single RCN-F1 vaccination (36 days after the first V-RG immunized subcutaneously. Thirty-day old red fox (Vul- vaccination {107 pfu}), nine of 10 treatment animals had pes vulpes) cubs with maternally derived antibodies from raccoonpox virus antibodies (range < 1:5 – 1:20; GMT = V-RG serologically responded (i.e., rabies virus neutraliz- 1:12), while three of 10 control animals had sera that was ing antibody {VNA}) to oral vaccination with V-RG [12]. reactive with this test (likely limited cross-reactivity of However, mice primed with avirulent ectromelia virus antibodies to the vaccinia virus in V-RG in some animals; survived a challenge with virulent ectromelia virus (genus range < 1:5 – 1:15; GMT = < 1:5). One animal was consist- Orthopoxvirus) with no signs of morbidity [13]. In mice ent with its background levels, but the titer of the other pre-immunized with vaccinia virus and subsequently vac- two animals increased. Ninety-seven DPI of the RCN-F1 cinated with a recombinant vaccinia virus, antibody titers vaccination, all treatment animals had positive raccoon- against the recombinant gene product were lower and pox virus antibody titers (range 1:5 – 1:15; GMT = 1:13), lasted for a shorter duration [14]. In contrast, similar stud- while the sera of four of 10 control raccoons were positive ies of adenoviruses suggested that the efficacy of oral vac- in this assay (range < 1:5 – 1:15; GMT = 1:6). The final cination is relatively unaltered by preexisting neutralizing detection for raccoonpox virus antibodies was performed antibodies to the vaccine carrier [15]. For vaccinia virus, on serum samples from 149 DPI of RCN-F1 vaccination the mechanism for such compromised immunity is (31 days following the second dose of V-RG {108 pfu}). thought to be associated with long-term anti-vaccinia Of the serum samples collected from that time point, all immunological memory, which inhibits the replication/ treatment samples were raccoonpox virus antibody posi- priming of the second vaccinia recombinant virus such tive and had identical titers to those samples collected at that the amount of the non-vaccinia antigen produced by 97 DPI (range 1:5 – 1:15; GMT = 1:13), while six of 10 the recombinant vector is no longer sufficient [14,16]. control samples had antibodies reactive with the test (range < 1:5 – 1:15; GMT = 1:7). The effects of pre-existing immunity on vectored vaccines have not been rigorously studied and different conclu- Rabies virus neutralizing antibodies sions have been drawn. Because this relationship has not Seven of the raccoons that were used in this experiment been thoroughly addressed for the oral vaccination of rac- had evidence of pre-treatment/natural rabies VNA (four coons, the objective of this study was to determine control and three treatment raccoons). The positive anti- whether exposure to raccoonpox virus inhibits the suc- body titers ranged from 0.20 – 0.80 IU/ml at that time. cessful V-RG vaccination and development of rabies VNA The titers of six of the seven raccoons (three of four con- titers in raccoons in an experimental pen setting. trol animals and all treatment animals) decreased in a subsequent serum sample. Prior to treatments being Results employed, the geometric mean titers (treating all < 0.05 Orthopoxvirus antibodies IU/ml titers as one significant digit less than the detection Pre-treatment serology indicated that seven (four control limit) were 0.10 and 0.08 IU/ml for the control and treat- and three treatment) of twenty raccoons may have been ment groups, respectively (Figure 1A). exposed to an orthopoxvirus prior to their capture, albeit Page 2 of 7 (page number not for citation purposes) BMC Immunology 2008, 9:57 http://www.biomedcentral.com/1471-2172/9/57 GraphicalimentcinationFigure (A), 1 representation36 days post first of rabiesV-RG virusvaccination neutralizing (B), 64 antibodies days post (VNA) first V-RG in raccoons vaccination duri (C),ng four and time 31 days points post including second pre-exper-V-RG vac- Graphical representation of rabies virus neutralizing antibodies (VNA) in raccoons during four time points including pre-experiment (A), 36 days post first V-RG vaccination (B), 64 days post first V-RG vaccination (C), and 31 days post second V-RG vaccination.
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