Canine rabies was reintroduced to the city of Arequipa, Peru in March 2015. The Ministry of Health has conducted a series of mass dog vaccination campaigns to contain the outbreak, but canine rabies virus transmission continues in Arequipa’s complex urban environment, putting the city’s 1 million inhabitants at risk of infection. The proximate driver of canine rabies in Arequipa is low dog vaccination coverage. Our objectives were to qualitatively assess barriers to and facilitators of rabies vaccination during mass campaigns, and to explore strategies to increase participation in future efforts. We conducted 8 focus groups (FG) in urban and peri-urban communities of Mariano Melgar district; each FG included both sexes, and campaign participants and non-participants. All FG were transcribed and then coded independently by two coders. Results were summarized using the Social Ecological Model. At the individual level, participants described not knowing enough about rabies and vaccination campaigns, mistrusting the campaign, and being unable to handle their dogs, particularly in peri-urban vs. urban areas. At the interpersonal level, we detected some social pressure to vaccinate dogs, as well as some disparaging of those who invest time and money in pet dogs. At the organizational level, participants found the campaign information to be insufficient and ill-timed, and campaign locations and personnel inadequate. At the community level, the influence of landscape and topography on accessibility to vaccination points was reported differently between participants from the urban and peri-urban areas. Poor security and impermanent housing materials in the peri-urban areas also drives higher prevalence of guard dog ownership for home protection; these dogs usually roam freely on the streets and are more difficult to handle and bring to the vaccination points. A well-designed communication campaign could improve knowledge about canine rabies. Timely messages on where and when vaccination is occurring could increase dog owners’ perception of their own ability to bring their dogs to the vaccination points and be part of the campaign. Small changes in the implementation of the campaign at the vaccination points could increase the public’s trust and motivation. Location of vaccination points should take into account landscape and community concerns.
The city of Arequipa, Peru is in the midst of an urban rabies epidemic. The first rabid dog was detected in March 2015, a rare instance of canine rabies reintroduction into an area previously declared free of transmission [1]. To date no human cases have been detected in Arequipa; however, continued transmission in dog populations puts the almost one million inhabitants of the city at risk of infection. Annual mass dog vaccination campaigns were instrumental in eliminating the disease from Arequipa in the 1990s. Unfortunately, this achievement was followed by low vaccination coverage in the years preceding the current outbreak [2]. Following the reemergence of the rabies virus in the city of Arequipa, the Ministry of Health of Peru (MOH) initiated additional vaccination campaigns with varying frequency [3]. These efforts have failed to quell the epidemic in Arequipa’s complex urban environment. Particularly, the city’s landscape is characterized by the presence of large dry water channels crossing the city in which free-roaming owned and stray dogs move, mix, and breed. Mass dog vaccination remains the most effective strategy to eliminate canine rabies and canine-mediated human rabies in developing countries [4–6]. In Latin America, a combination of intensive dog vaccination and surveillance efforts has produced dramatic decreases in canine and human cases [5]. However, in addition to reintroduction in Arequipa, canine rabies has been recently introduced to new areas in Latin America such as Jujuy and Salta in Argentina, Mato Grosso do Sul in Brazil and Loma Plata in Paraguay [1]. New efforts and strategies to control the disease in the region are critical. Eliminating canine rabies is feasible; however, several attempts based on dog vaccination have failed to achieve adequate coverage in the Americas, Africa and Asia [5,7, 8]. There are multiple potential drivers of low participation in vaccination campaigns in southern Peru and elsewhere. The social ecological model [9] is a theory-based model that recognizes the complexity of the socio-cultural system in which individuals make decisions and take actions. This theory emphasizes that individuals not only make decisions based on their own knowledge and experience (individual level factors), but are also influenced by their interpersonal relationships (e. g. norms, families and peers), organizations (e. g. health promotion and prevention activities of health services), their community (e. g. physical environment), and policies (e. g. national or state laws) [9]. At the individual level, the ability to restrain and handle dogs [10–15]; lack of time to attend vaccination campaigns [12,13,15]; lack of information [10,13–15]; and level of knowledge of rabies [14,16–20] have been shown to influence vaccination uptake. At the interpersonal level, social norms (i. e. those affecting dog ownership practices) and migration patterns can have a distinct impact on people seeking preventive services, such as vaccines for their dogs [21–25]. At the organizational level, location and number of rabies vaccination points may be particularly important [11,15,16]. Also, the quality and quantity of health messages about rabies and the rabies campaigns may impact people’s knowledge, but not necessarily their behaviors [26]. At the community level, distance and topography can act as barriers to providing and accessing health services in urban and peri-urban settings [27–30]; in rural settings in particular, distance has been reported as a barrier to achieving high dog rabies vaccination coverage [11,15,16,31]. At the policy level, efforts to eliminate canine rabies have been jeopardized by lack of funding and low political will [5,32]. In Peru, the MOH organizes annual mass canine rabies vaccination campaigns in all cities (affected and unaffected by canine rabies). Campaigns are held on either one or two weekend days, offer free vaccination in outdoor settings, and are voluntary. The MOH uses a cell-culture-based vaccine [33]. Campaign promotion is conducted at the local level, primarily via posters placed in health centers, corner stores, schools and other meeting places a couple of weeks or a few days before mass vaccination. The day before and the same day of mass vaccination, campaign staff promote the campaign on foot or from trucks using megaphones; their routes are somewhat haphazard. Locations of the vaccination points are determined a few days in advance; some locations are relatively permanent from year to year (e. g. the entrance to a health post), whereas others may be selected on the day of the campaign. Teams may also move during the course of the day from a lower-demand to a higher-demand location. Vaccination usually starts between 8: 30 and 10: 00 am, and ends between 1: 00 and 3: 00 pm. The dog population (coverage denominator) is estimated based on the human: dog ratio method. The true human: dog ratio is highly variable geographically [34] and the ratio used throughout Arequipa has been changing from 10: 1 to 5: 1 in the last two years making vaccination coverage estimation a fast moving target. The reemergence of rabies in the city of Arequipa has been associated with low dog vaccination coverage [2] and a high density of free-roaming dogs (i. e. stray and owned dogs that spend unsupervised time in the streets and water channels) [2,3]. The social and physical aspects of urbanization in rapidly growing cities such as Arequipa may also facilitate the emergence of canine rabies and complicate its control [35–39]. Epidemics of rabies and other zoonotic pathogens are ongoing in major urban centers across Latin America and worldwide [5,40–46], and it is necessary to understand barriers to dog vaccination, as well as to assess people’s understanding of rabies transmission and prevention. The objective of this study was to qualitatively assess barriers to and facilitators of dog vaccination during the mass campaigns implemented by the MOH in Arequipa, Peru, as well as to explore strategies to increase participation in future campaigns.
Institutional Review Board approval was obtained from Universidad Peruana Cayetano Heredia (approval identification number: 65369), Tulane University (approval identification number: 14–606720), and University of Pennsylvania (approval identification number: 823736). The study was conducted in the Mariano Melgar district (pop. 55,000) of the city of Arequipa, Peru’s second largest city. Arequipa is home to 969,000 people [47], and is situated at ~2,300 meters above sea level. The first detection of a rabid dog in the city of Arequipa occurred in March 2015 and by January 2016 (when our data were collected), 20 rabid dogs had been detected, of which 11 were found in Mariano Melgar. The city of Arequipa comprises communities spanning different stages of urbanization and different migration histories, from old established neighborhoods, to young neighborhoods, to recent invasions [48]. Within this gradient of development, young neighborhoods and recent invasions are often located on the periphery of the city (peri-urban area) and the older localities are nearer to the center (urban area) [38]. Compared to the urban area, peri-urban areas generally have lower socioeconomic status, fewer community resources, more security problems, and often more rugged and uneven terrain (Fig 1). As new neighborhoods mature into established neighborhoods with wealthier residents, homes are improved with better quality construction material and permanent utility connections, and connectivity with the rest of the city increases with better sidewalks, roads, and transportation access. One of Arequipa’s 14 districts, Mariano Melgar transects the city, running from the center to the periphery; the district continues to grow towards the outskirts of the city. In our study, participants represented either the urban or peri-urban areas of the city of Arequipa. The urban neighborhoods were founded several decades ago, while the peri-urban neighborhoods in our study originated around 2000 or later. Purposive sampling was used to select participants for a series of eight focus groups (FG). All participants were residents of urban and peri-urban neighborhoods and were recruited according to their geographic proximity to the site where the focus groups were held. To ensure that participants were not overly exposed to health promotion messages (i. e. posters about rabies vaccination campaign) or activities from a nearby health facility, all participants were recruited from homes located at least 6 blocks from the district' s municipal building and health posts. The population in the Mariano Melgar district that lives 6 blocks or further from a health post or the municipal building was approximately 45,256 people. All participants in each focus group lived in the same neighborhood, but were recruited to represent a range of ages, gender, dog ownership (i. e. most participants had dogs, but in each FG we tried to have one person who did not currently own a dog), and dog vaccination status (i. e. we aimed to include both dog owners who had and had not participated in the vaccination campaigns in each FG). Research team members recruited participants door-to-door one day prior to the focus group. Pre-selecting blocks from a map, research assistants visited every third house within a block until they identified 2 or 3 individuals 18 years or older, preferably a dog owner, who were willing to participate. The same strategy was applied to all selected blocks until 15 individuals were invited to each focus group, to ensure a target attendance of 8–12 participants. The recruitment team explained the study goals and obtained written informed consent from all eligible participants. The recruitment team made follow-up visits the next day 45 minutes before the agreed-upon focus group time to remind participants. Consenting participants were picked up by car from their homes 10 to 15 minutes before the beginning of the FG and taken to the FG location. Participants were compensated for transportation home. Seventy individuals (18 to 81 years of age) participated in eight FG (4 groups each in the urban and peri-urban communities) over four days. The majority of participants were female (n = 54), but all focus groups had female and male participants (Table 1). FG guides were developed to cover four topics: dog ownership, dog ecology, and barriers to and facilitators of dog vaccination. Four facilitators conducted the FG: a social scientist experienced in qualitative research (VPS, PhD in public health), a research assistant (JB, BA in psychology), an infectious disease scientist (RCN, veterinarian and PhD in epidemiology, lead investigator of the study), and a note taker. All facilitators were Peruvian, and the infectious disease scientist has lived and/or worked in Arequipa for more than seven years. All FG discussions were digitally audio-recorded and transcribed, and detailed notes were taken throughout. An inductive coding process was used: we first grounded ourselves in the data to explore the topics that would emerge, not knowing what to expect [49]. Codes were then developed based on the emerging themes. Data were imported into ATLAS. ti [50] and coded by two members of the research team; any inconsistencies in the coding were discussed thoroughly until agreement, with codes added as needed. Transcripts that had been coded were recoded with the revised coding scheme. To address the main question of interest to the researchers, all data coded to themes related to canine rabies vaccination barriers and facilitators were summarized, stratified by urban vs. peri-urban communities, and younger (<30 years of age) and older participants.
Various theories have been developed to guide assessments of effectiveness of rabies vaccination campaigns [10,52,53]; an important component of this work is examining the perspectives of dog owners and community members, both qualitatively and quantitatively [53]. This article analyzes unique focus group data, and is the first from our ongoing multi-method studies of factors associated with coverage of and participation in mass canine rabies vaccination campaigns. The social ecological model [9] applied here to structure the themes raised by FG participants is a theory-based model that recognizes the complexity of the socio-cultural system in which individuals make decisions and take actions. Our findings reveal multiple barriers to dog vaccination at the individual, interpersonal, organizational and community levels of the social ecological model. We identified individual-level barriers to vaccination as well as facilitators of vaccination. An important next step is to translate these barriers and facilitators into proposed solutions to improve campaign effectiveness, using evidence-based concepts from health behavior change theory. For example, our respondents suggested using fear-based promotional materials and punishments for non-participation. This proposed solution highlights the importance of self-efficacy (the self-perceived ability that one can practice a proposed solution) as a driver of health behavior, as posited in several health behavior change theories, including the extended parallel processing model (EPPM) [54]. The EPPM model proposes that when faced with a health risk, people will take actions to protect their health if they are empowered by an appropriate balance of fear and self-efficacy [54], consistent with other models that predict adverse consequences from employing fear in health communication programs without assuring high self-efficacy levels [55–58]. A health communication campaign that focuses on instilling fear alone will often result in a feeling of helplessness and inaction. However, communication that conveys risk in an understandable way and also provides a clear and do-able call to action to reduce one’s risk leads to empowered citizens who take action [59]. Rabies is a fatal and devastating disease and Arequipa is facing a sustained rabies outbreak that has not yet been controlled, posing a serious risk for humans and animals; vaccinating one’s dog is a highly effective prevention method that only requires dog owners’ efforts once a year. Rabies vaccination communication should tap into this feeling of risk (to increase individuals’ perceived susceptibility to rabies, and inform them of the severity of this virus), while at the same time help individuals feel confident in being able to act (self-efficacy in handling their dogs and participating in campaigns) to effectively mitigate that risk. This communication should not only address knowledge gaps, but also inspire trust in the program and emphasize motivators that participants described, including keeping one’s family healthy, protecting the household pets from rabies, and keeping the community free of rabies. A very salient individual level barrier mentioned in FG was the logistics: difficulty getting dogs to vaccination sites, dog fights en route to and at the vaccination points. To a certain extent, this barrier can also be mitigated through improvements to the rabies vaccination program. Other Latin American countries have taken steps to improve people’s ability to handle their dogs. For instance, Costa Rica included in their “Guidelines of Pet Reproduction and Ownership” to walk dogs on the leash frequently to increase their proper socialization [60], and new Mexican bills support citizens’ initiatives to adequately integrate dogs in society, such as the “Social Dog, Responsible Owner Program” [61], which provides training to dog owners and their dogs through in-person workshops, online videos, and written material. Based on our findings, to address some of the knowledge gaps in the population that could deter vaccination for some dogs, health communication campaigns should include additional information about when one should vaccinate one’s dogs and describing that all dogs (even those that are always indoors) are at risk. At the interpersonal level, barriers discussed by participants were related to the social norms of poor animal care culture in Arequipa, competing social pressure both for and against vaccination, although the latter was considerably less common. Most respondents in this study also indicated that there is social pressure in Arequipa for people to vaccinate dogs, as those who do not vaccinate are seen in a negative light; they are considered lazy, uncaring for animals, and irresponsible neighbors in the context of community protection offered by vaccines (although a few also described social pressure to not vaccinate—feeling laughed at for spending time and/or money on a dog). The theories of diffusion of innovations [62], social learning [63] and planned behavior and reasoned action [64] point to the importance of social norms, the opinion of others, and social networks in making decisions about health behavior. Vaccine promotion communication in Arequipa should be informed by these theories and seek to influence local norms by providing information from trusted and influential sources, as well as identifying well-connected individuals in communities to champion certain ideas—including but not limited to local storekeepers, health workers that routinely work in certain areas, health care providers (i. e. veterinarians), local neighborhood authorities, municipal governments, health officials, local celebrities, teachers, and respected elders. Barriers that emerged at the organizational level were health system weaknesses, such as insufficient promotion of the vaccination campaign, poor selection of location for the vaccination points, low frequency of vaccination campaigns, and insufficient staff during the campaign. Regarding the service, trust in quality of services can be improved through strategic decisions and actions in the implementation phase. Identification cards with the vaccinator’s name and qualifications should be visible to campaign attendees—both on the vaccinator and on any visible media (e. g. posters, banners) at the site. Likewise, keeping coolers visible and less exposed to the sun might help increase confidence that the cold chain has been kept intact, showing the unopened syringe or needles before filling them would quell rumors of syringes are reused, and pointing out the expiration date on the vaccine vials before filling the syringe would take seconds, but increase trust in the product. Finally, a barrier mentioned in many FG was the insufficient or untimely information about date and locations of vaccine campaigns. This barrier can also be addressed in the planning and implementing phases: announcements about the campaign can start earlier and through different media, and be conducted on different weekdays and times, to ensure more people hear about them. Posting times, dates, and locations of upcoming vaccination campaigns in advance and in visible community locations would also allow for individuals to plan where and when to take their dogs for the vaccination, and to plan to have extra people to help take the dogs if necessary. Participants mentioned other health programs based on door-to-door interventions such as the Chagas control campaign that could have lessons to offer the rabies campaign. Door-to-door strategies have been discussed among local officials to promote participation and also enable a simultaneous canine census to improve the accuracy of coverage data. These and other interventions at the organizational level to improve rabies vaccination uptake can be modeled according to the health care access framework presented by Obrist et al. [52]. This framework consists of five dimensions: availability, accessibility, affordability, adequacy, and acceptability; the present study provides insights into each of these dimensions. At the community level, barriers cited included distance to vaccination points, difficult topography (particularly in the peri-urban areas), and lack of security in the area. Flexible strategies are necessary to meet the local community needs [11,16]; for instance, in rural Tanzania [11], a few central-point canine rabies vaccination points were insufficient to achieve 70% coverage (WHO recommended threshold), and had to be supplemented by door-to-door efforts [65]. The combination of central-point and door-to-door dog vaccination has also proven to be effective in urban environments, with one large city recently achieving 79% coverage [66]. Participants’ preference for door-to-door campaigns is also important to highlight: this has usually been done in rural areas [11,66], and although the topography and urban design in some cities is ideal for centralized vaccinations, clearly not all urbanized settings are the same: a central-point mass vaccination campaign in the urban areas of N’Djamena, Chad achieved a coverage above 70% [67], while a similar central-point vaccination campaign in the city of Bamako, Mali achieved only 17% coverage [10]. In our study, campaigns in the urban areas were fairly accessible to dog owners (despite having to cross large avenues), but the topography of the peri-urban areas was much more difficult (steep hills, large rocks, unpaved roads) for people trying to get multiple unleashed dogs to vaccination points. Rapid urban spread, low salaries, scarce resources and bureaucratic rules can all impede the responsiveness and quality of campaign services [68]. For rabies, control programs must take into account social, political and cultural contexts to improve efficacy and avoid the barriers faced by other top-down public health interventions [69–71]. Our study and others [16–18,26,72–74] have focused on dog owners’ knowledge, dog-ownership practices, norms, and perceptions about the dog vaccination campaign as important factors to understand the rabies program’s outcomes. But capacities, norms, and policies of implementing institutions also play a central role in rabies control efforts [16]. Overall, although some of the suggestions discussed would add to program expenses, several imply little marginal cost; many suggested strategies simply optimize current investments for better efficiency. For example, current promotional materials could be more informative (i. e. include location and hours of vaccinations) and be disseminated earlier; vaccinators could visibly display their ID and credentials; and vaccine syringes could be opened in front of dos owners with additional explanations about safety and quality procedures to increase trust in the campaign. Similar to prior studies [74], we found different attitudes, dog-ownership practices, and knowledge levels between urban and peri-urban areas. Given the different characteristics of these areas (topography, migration history, level of urbanization, levels of security and utilization of dogs for companionship vs. protection), it is difficult to justify a one-size-fits-all campaign strategy. The newer peripheral communities we studied in Arequipa are typical of peri-urban areas, a neglected zone in Latin America, Africa, and Asia [75] commonly characterized by inadequate infrastructure, service provision, and land tenure security [38,76]. While most public health campaigns have distinct strategies for urban vs. rural areas; the peri-urban area (or rural-urban interface), one of the fastest growing areas in the world [75], lacks a specific and responsive programmatic approach in Peru and elsewhere.
Important individual, interpersonal, organizational, and community level factors limit more widespread participation in dog rabies vaccination campaigns in the city of Arequipa–site of a canine rabies outbreak since 2015. A comprehensive communication campaign is required to increase the population’s knowledge about rabies’ transmission, its consequences, and prevention measures. Developing strategies to help dog owners not accustomed to using leashes should be explored and implemented to help facilitate the transport of dogs to vaccination points. It is important to provide timely information about free dog mass vaccination campaigns. Clear identification of vaccinators and demonstration of unopened needles and syringes, as well as training vaccinators on their interactions with dog owners and response to their concerns can also help increase trust in the campaign. Finally, flexible strategies are needed to serve diverse communities within a city; urban and peri-urban areas present contrasting landscapes that might require different vaccine point locations.
Canine rabies was reintroduced in Arequipa, Peru in March 2015, a rare event in an area previously declared free of transmission. In Arequipa, annual mass dog vaccination is practiced as a preventive strategy, with additional campaigns being implemented since the recent detection of the virus. However, these additional efforts have not quelled the outbreak and low dog vaccination coverage is driving ongoing transmission. We conducted focus groups in urban and peri-urban areas of Arequipa to identify barriers to and facilitators of canine vaccination during mass campaigns. Based on our findings, communication campaigns should seek to increase knowledge about canine rabies and the vaccination campaign, and provide timely messages on where and when vaccination is occurring. Small changes at the campaign’s vaccination points could increase public’s trust. Finally, there are differences between urban and peri-urban areas, such as landscape and topography that affect participation in mass vaccination campaigns and that should be considered when selecting locations for vaccination points.
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Barriers to dog rabies vaccination during an urban rabies outbreak: Qualitative findings from Arequipa, Peru