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Investigations Into the Physiological And INVESTIGATIONS INTO THE PHYSIOLOGICAL AND BIOMECHANICAL BASIS OF DIFFERENTIAL SUCCESS IN ORAL RABIES VACCINATION BETWEEN SKUNKS (MEPHITIS MEPHITIS) AND RACCOONS (PROCYON LOTOR) A Thesis Presented to the Honors Tutorial College Ohio University In Partial Fulfillment of the Requirements for Graduation from the Honors Tutorial College with the degree of Bachelor of Science in Biological Sciences by Charlotte M. Klimovich August 2017 2 Table of Contents INTRODUCTION ........................................................................................................................... 3 EXECUTION OF ORAL RABIES VACCINATION PROGRAMS .................................................. 4 HISTORY OF DISEASE CONTROL PROGRAMS ........................................................................ 5 A NEW ERA OF DISEASE CONTROL .......................................................................................... 7 OPTIMIZATION OF ORAL RABIES VACCINE PROGRAMS ...................................................... 9 PROJECT HYPOTHESES AND OBJECTIVES ........................................................................... 12 AIM 1: FACTORS INFLUENCING BITE FORCE PRODUCTION CAPABILITIES AT DIFFERENT GAPES USING BIOMECHANICAL MODELS INFORMED BY JAW MUSCLE AND SKELETAL STRUCTURE ................................................................................................... 19 Background and Hypotheses ......................................................................................... 19 Materials and Methods ................................................................................................... 26 Results ........................................................................................................................... 32 Discussion ...................................................................................................................... 37 AIM 2: COMPARE NATURAL BITE FORCES AT DIFFERENT GAPES IN LIVE ANIMALS .. 40 Background and Hypotheses ......................................................................................... 40 Materials and Methods .................................................................................................. 41 Results ........................................................................................................................... 43 Discussion ...................................................................................................................... 45 AIM 3: EVALUATE DIFFERENCES IN ORAL HANDLING, MASTICATION, AND SWALLOWING OF THE SACHETS USING BIPLANAR FLUOROSCOPY ............................... 47 Background and Hypotheses ......................................................................................... 47 Materials and Methods .................................................................................................. 48 Results ........................................................................................................................... 50 Discussion ...................................................................................................................... 55 SYNTHESIS .................................................................................................................................. 57 REFERENCES ............................................................................................................................. 62 APPENDIX 1................................................................................................................................ 69 3 INTRODUCTION A raccoon rabies variant (RRV) epidemic has been raging on the east coast of the United States since the 1970s (Anonymous 2000). Over 90% of all rabid animal cases reported to the Centers for Disease Control and Prevention (CDC) in modern times occur in wild animals. Rabies used to be rare outside of the Southern United States, but uncontrolled outbreaks in wildlife are now placing unprecedented numbers of citizens at risk of exposure. An increase in prophylactic rabies treatments given due to possible exposures indicates the seriousness of this issue; while fewer than one hundred treatments were given in the entire state of New York before 1990, more than 10,000 are now given annually. The epidemic had spread from Florida to West Virginia by 1984, when the first oral vaccine (V-RG, now called RABORAL V-RG) was created (USDA 1995). The CDC spends more than $300 million a year attempting to contain RRV and the other rabies variants found around the United States (Centers for Disease Control and Prevention. 2015). Oral rabies vaccination (ORV) programs have been shown to be effective in many species, with reported cases decreasing in all animal species measured during 2010 (Blanton et al. 2011). However, the CDC must constantly develop and implement new techniques to keep up with the changes in both the disease itself and the way it is transmitted to ensure the numbers of rabies cases found annually continue to decrease. 4 EXECUTION OF ORAL RABIES VACCINATION PROGRAMS The RRV ORV program utilizes sachets of liquid RRV vaccine covered by an attractant such as fishmeal (Anonymous 2000). In the United States, these sachets are produced by Merial (Duluth, Georgia). They are distributed by plane or vehicle, depending on the density of humans in the area. When animals find the vaccine bait, they eat it and ingest liquid vaccine. Virus in the liquid absorbed through the oropharyngeal mucosa will penetrate the lymphoid tissue, including the lingual and palatine tonsils, lining the opening of the Figure 1. Example of a fishmeal polymer oropharynx and induce the Raboral V-RG bait. production of rabies antibodies that enable the animal to mount an immune response in case of exposure (Brown et al. 2014). Raccoon (Procyon lotor) populations have satisfactory rates of immunization from oral vaccination using the sachets (Roscoe et al. 1998). It is commonly accepted that around 70% of animals in a population should be immunized to effectively control transmission of a disease, with evidence from both practice and theory supporting this percentage (Zalma, Older, and Brooks 1970; Simonsen et al. 1987). However, oral rabies vaccination of raccoons is not infallible. For example, in 2004, a raccoon was found in Lake County (Ohio) with rabies strain later shown to have originated from within the 'rabies-safe' zone created by the ORV program (Henderson et al. 2008). This means that enough rabid raccoons had survived within the zone to create a distinct strain of rabies virus - quite the opposite of what the CDC had intended (Klimovich 2013, unpublished data). 5 In contrast, 2010 census data from the Centers for Disease Control and Prevention show that skunks (Mephitis mephitis) are unresponsive to ORV programs (see (http://www.cdc.gov/rabies/location/usa/surveillance/wild_animals.html). The striped skunk is second only to the raccoon in number of rabies cases reported and there is evidence that RRV (usually only found within the raccoon population) is now endemic in the skunk population (Guerra et al. 2003). Host shifts are associated with the emergence of some of the most virulent infectious diseases in humans including AIDS, SARS, swine flu, and Ebola, so it is imperative to explore new methods of control before a large-scale public health threat emerges from the disease running rampant in the skunk population. It remains unclear why the response to oral vaccination differs between skunks and raccoons. Other studies have analyzed bait distribution strategies, bait campaign timing, natural barriers, gender, age, population density, eating behaviors, bait color, bait odor, and bait texture to offer suggestions about ways to improve efficacy (Robinson, Jojola, and VerCauteren 2004; Jojola, Robinson, and VerCauteren 2007; Feldhamer, Thompson, and Chapman 2003; Greenwood 1980). Even using improved baits, however, immunization rates in skunks still remain low (Fehlner-Gardiner et al. 2012; Mainguy et al. 2012; Tolson et al. 1987). HISTORY OF DISEASE CONTROL PROGRAMS In the process of exploring options to vaccinate skunks, it is beneficial to understand the evolution of oral rabies immunization programs in raccoons over time in order to inform possible skunk ORV development. Prior to 1950, raccoon rabies was not reported as a problem in the United States. The first increase in numbers of rabid raccoons occurred between 1950 and 1970, mostly in Florida and Georgia. The rabies 6 variant implicated in the current outbreak was detected in 1977 in Virginia and West Virginia, marking it as separate from the rabies strain observed in Florida and Georgia, although they eventually converged into one rabies strain (Anonymous 2000). There is evidence that this 1977 rabies variant appeared due to translocation of an infected raccoon from the southeastern United States to the region (Jenkins and Winkler 1987; Nettles et al. 1979; J. S. Smith et al. 1984). There were many possible options to control the spread of this disease. One common historical technique to control rabies was population reduction, as it was believed that a certain number of animals are required to effectively pass rabies through the group (Debbie 1991). This approach has not been popular due to impractical cost and predicted impacts on nontarget species due to the techniques employed (such as hunting, poison baits, gassing, and trapping) (Debbie 1991; MacDonald and Research 1980). Habitat modification is a similar technique that is often used in site specific
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