Rocky Mountain spotted fever (RMSF) is a severe and potentially fatal tickborne disease caused by the bacterium Rickettsia rickettsii. This intracellular bacterium can cause widespread vasculitis resulting in organ failure and death if left untreated, even in previously healthy individuals [1]. Thousands of cases of RMSF are reported annually to the Centers for Disease Control and Prevention (CDC) from across the United States, with the majority of cases originating from the South-Atlantic states [2]. From 2009–2012, the average annual incidence of RMSF in the United States was around 0.9 cases per 100,000 persons [3]. In the United States, RMSF is most commonly transmitted by the American Dog tick (Dermacentor variabilis), which is widely distributed east of the Rocky Mountains, and on the California coastline. It is also transmitted by Dermacentor andersoni (the Rocky Mountain wood tick) in the western United States. Both of these tick vectors prefer wooded areas and acquire the majority of blood meals from wildlife [4].

The dry, hot Arizona weather is inhospitable to the temperature and humidity requirements of Dermacentor ticks, so the risk of contracting RMSF within the state was considered to be low. From 1988 to 2003 only eight cases of RMSF were reported in AZ, most acquired outside the state [5]. However, from 2003 until 2012 the Arizona Department of Health Services (ADHS) reported over 250 cases of RMSF and 19 fatalities, almost all among American Indians without a history of travel [5]. On the three most heavily impacted reservations, the average annual incidence for 2009–2012 was ∼136 cases per 100,000 persons, over 150 times the national average.

Following epidemiologic and ecologic investigations, the dramatic increase in autochthonous RMSF cases in Arizona was linked to transmission by the brown dog tick (Rhipicephalus sanguineus sensu lato) [6]. Although this tick species is prevalent throughout the world, the Arizona outbreak was the first time this tick was shown to transmit RMSF infection in the United States. Dogs are the primary host for this tick species at all life stages, and provide both the primary food source for the tick and sites for adult ticks to mate [7]. Dogs are susceptible to infection from R. rickettsii and may influence bacterial infection rates in local tick populations [8]. Based on high rates of seropositivity in dogs, the burden of tick parasitism of ticks on dogs, the evidence of R. rickettsii bacteremia in some sick dogs with heavy tick burdens, and the abundance of free-roaming dogs in this area, it is likely that dogs serve as a major amplifying host for R. rickettsii in this area, although wildlife evaluations have not yet occurred [6], [8]–[14].

In regions where RMSF is primarily associated with Dermacentor ticks, RMSF prevention largely centers on human behavior changes and personal protective measures, in order to avoid traditional tick habitats and tick bites. Such activities include wearing light colored clothing, using repellents containing DEET when in contact with wooded areas and high brush, and staying to the inside of trails [15]–[22]. However, such practices are not applicable for avoidance of the brown dog tick, which is found primarily in domestic and peridomestic settings. Because avoidance behaviors do not work in a scenario where constant exposure is likely, preventing Rhipicephalus-transmitted RMSF requires control of ticks on dogs (the primary food source) and in the peridomestic environment (the primary location for non-feeding ticks).

In order to determine if brown dog tick control could be attained in a heavily infested community, we designed and evaluated an intervention aimed at killing ticks on dogs and in the peridomestic environment using properly timed environmental acaricide application and long-acting tick collars for dogs.

Within the RMSF Rodeo community, 98% (576/582) of occupied households in 2012, and 99% (558/571) of occupied households in 2013 participated in the intervention project. Although defining a precise number of dogs was difficult due to births, deaths, loss, and transfer of ownership; we estimate that roughly 1000 dogs were managed within the RMSF Rodeo community each year, but that number fluctuated by month.

The RMSF Rodeo tick prevention project successfully decreased tick levels within this tribal community, and maintained low levels of ticks for a period of at least two years. In the first year, environmental tick control methods combined with long-acting tick collars on dogs produced substantially fewer domestic and peridomestic infestations in the RMSF Rodeo community compared to the Non-Rodeo communities, as evidenced by observed tick activity on dogs, environmental CO₂ traps, and homeowner reports of sighted tick activity. Once tick control had been achieved during Phase 1 of the RMSF Rodeo, using the combined environmental and veterinary tick control, tick populations were sustained at very low levels during Phase 2 of the RMSF Rodeo using tick long-acting collars alone.

We believe that the success of the RMSF Rodeo was due to the tailoring of interventions around this tick vector and its particular habits. The start of the project in March-April of each year was timed to correspond with human RMSF surveillance data showing increased cases during those months, presumably due to increased tick activity [7], [31], [32]. Use of properly timed environmental acaricides with repeated applications during Phase 1 allowed for the control of hatched ticks in the environment at several points during the year. The simultaneous placement of a long-acting tick collar prevented community dogs from becoming both the food and reproductive resource for this tick vector. Evidence indicates that at the individual dog level presence of a tick collar was highly associated with absence of ticks, and in 2013, un-collared dogs were more than five times as likely to have visible tick infestation as collared dogs. This suggests that presence of the collar is a pivotal factor in the individual and likely community-wide control of ticks. Always restraining dogs was seemingly protective of observed tick activity, and never restrained dogs were at increased risk of having observable ticks. Previous studies have shown that restrained dogs are more likely to have tick infestations than unrestrained dogs, presumably because of high levels of local environmental infestation, and because they are easy prey for meal-seeking ticks [33]. However in this case, where concurrent yard treatments were used in addition to collar treatments, we believe unrestrained dogs were more likely to travel to untreated (non-peridomestic) areas or interact with other, non-treated dogs, thereby increasing their risk of tick infestation.

Another important factor in the success of the project was the strong degree of support for the RMSF Rodeo within the community, as demonstrated by the high rate of household enrollment. Households were visited multiple times and registration was repeatedly encouraged in order to procure this high rate of participation, which was crucial in the project's ultimate success.

The finding that ticks were controlled across the community during Phase 2 of the project using tick collars alone is very promising. Even though Phase 2 of the project included a contingency for acaricide treatment in the project area for households where tick activity was observed, this was necessary in <5% of households in the RMSF Rodeo community, suggesting that the tick collar alone was sufficient in preventing the majority of visible tick infestations on dogs once environmental burden was reduced. This method enables more targeted and cost-efficient strategies of tick control, interceding on the primary host, and will reduce the amount of pesticides necessary in the environment.

The RMSF Rodeo project did not evaluate the efficacy of a tick collar alone during Phase 1 of the project, and we do not recommend this option for communities with high environmental tick loads. We believe rapid and immediate killing of ticks in the environment is essential to reduce RMSF risks in highly impacted communities. There is also a possible risk: if collars are used without controlling ticks in the peridomestic environment, meal-seeking ticks may be inclined to parasitize other unprotected animals in the immediate area including humans. Thus, during a period of initial tick control, we recommend a combined approach that includes environmental treatments.

The RMSF Rodeo was not designed to compare the efficacy of different tick control products. Seresto collars were selected because they provided a visible marker of dog treatment, were easy to apply, and represented the longest-acting product of this type with market approval. Similarly, the Bayer Advanced environmental acaricide was used because it was donated by the company, but also because it could be purchased and applied by homeowners without special licenses in the future. It is possible that similar tick control could also be achieved using different products; however, product longevity and effectiveness should be considered when selecting products.

This pilot project is subject to some limitations. Survey answers are subject to recall bias and interpretation, as well as perceived pressures to provide socially acceptable answers. Respondents in the RMSF Rodeo community may have felt a greater need to provide responses which inflate the project's success out of courtesy to the interviewer, which would bias our results away from the null. Neighborhoods were separated into intervention (RMSF Rodeo) and non-intervention (Non-Rodeo) communities; however, in some unusual cases we found RMSF Rodeo collars on dogs in Non-Rodeo communities, as a result of sharing of products between family members or translocation of dogs. While RMSF Rodeo and Non-Rodeo communities were geographically isolated from one another, unrestrained dogs may also have traveled outside of their intervention area or been translocated by human activity. These occurrences could result in spill-over between intervention and non-intervention communities, and may have introduced a bias towards the null hypothesis. Despite best efforts, dogs had the potential to be lost or duplicated among program records. Longitudinal analysis of all enrolled dogs was not possible as dogs were continually enrolled, died, or changed locations and identification tags were lost and duplicated; therefore, only cross-sectional data are reported. Our final limitation was the inability to track the Non-Rodeo areas for a second year to serve as a control group. Due to the overwhelming success of the RMSF Rodeo in 2012, the tribe implemented a modified tick control program in Non-Rodeo areas in 2013.

Reducing RMSF cases among tribal residents is the primary goal of the RMSF Rodeo. Control of tick activity in domestic and peridomestic locations is expected to reduce the risk of human exposure to R. rickettsii carrying ticks, but measuring the effects on human incidence is difficult to document. Before the start of the RMSF Rodeo there was high incidence of RMSF among residents of the RMSF Rodeo and Non-Rodeo communities. In the two years following the start of the intervention, decreases in human incidence were observed across the reservation; however a more substantial decrease was noted in the RMSF Rodeo community. The significance and attribution of the observed decrease, however, is uncertain, and we believe that it will take several more years to fully measure the impact of this project. Reported human cases of Rocky Mountain spotted fever fluctuate widely year to year, and are influenced by human exposure patterns and testing and reporting practices [2]. Due to the relatively new emergence of this disease in Arizona, trends in disease occurrence are not yet well established, and may be influenced by factors such as rainfall and temperature, which vary from year to year [34]. Tribal residents frequently travel in between communities and may be exposed to ticks elsewhere on the reservation, so location of residence does not necessarily correspond to location of exposure. Reduction in human cases in the Non-Rodeo areas may be due to annual variation, but could also be ascribed to reservation-wide RMSF control efforts including improved animal control, provision of spay and neuter services and reservation-wide collaring and environmental acaricide treatment beginning in 2013. Finally, diagnosis of RMSF was frequently based on detection of antibodies in single serum samples, and in high-incidence areas a high percentage of the population may be antibody-positive from past exposures, rather than new acute infections [35]. We plan to continue tracking human cases using surveillance data and working with physicians and local public health authorities to improve the case confirmation process to better document human cases of RMSF in these communities and evaluate long-term changes in incidence.

Since the development of this project, the need for Rhipicephalus-transmitted RMSF prevention has only grown. There are now six American Indian reservations in Arizona with documented human cases of RMSF, placing more than 350,000 American Indians at risk for this deadly disease [30]. The evidence obtained in this project has been used to generate RMSF prevention strategies for other Arizona tribes considering RMSF prevention programs, and has informed the substantial effort and vigilance that must go along with continued RMSF prevention within the state.

While the 2-year RMSF Rodeo program achieved a remarkable degree of tick control, it is worth noting that ticks were not completely eliminated in the RMSF Rodeo community. Tick control efforts will need to be maintained in coming years in order to keep the risk of tick bite and RMSF reduced in this community. It is unlikely that a full elimination scheme can be achieved for such a ubiquitous pest. However, it is the hope that adequate tick control in the environment and on animals will decrease the opportunities for human illness, and, when coupled with supportive care from well-trained physicians, cases can be caught sooner and deaths prevented.