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Introduction
Foot-and-mouth disease (FMD) is a highly contagious viral disease of livestock caused by an Aphftovirus affecting cattle, swine, sheep, goats, and other cloven-hoofed ruminants. It is characterized by fever and blister-like sores on the mouth, teats, and between the hooves (Blood et al., 2002). FMD has a large economic impact on animal production ( Casas Olascoaga et al., 1999; Knight-Jones & Rushton, 2013), with costs not only limited to direct losses but mainly associated with indirect costs on control strategies and access to high price exporting markets (MGAP, 2019).
Uruguay’s FMD outbreaks in 2000 and 2001 shook the Uruguayan livestock sector with losses of more than 700 million USD (Antunez, 2019, May 22). Veterinarians play a key role in the early detection and disease control strategies, aiding in reducing the economic impact. Suspected clinical cases must be reported to the National Animal Health Services who will visit the farm and carry out a comprehensive epidemiological study. Thus, veterinarian’s perception on FMD control strategies may have a role on early disease detection on the field.
There are seven strains (A, O, C, SAT1, SAT2, SAT3, and Asia 1) which are endemic in different countries worldwide, but in this century, for Uruguay only strains “A” and “O” are relevant. The strains present in a particular region must be taken into account for defining vaccination strategies, and vaccine composition. Also, depending on the country and epidemiology situation, not all susceptible animals should be vaccinated. For example, in Uruguay, only cattle are vaccinated while other species remain susceptible to the virus (COSALFA, 2019; Paton et al., 2018). These vaccination characteristics might impact veterinarian’s perception on the effectiveness of control strategies.
Argentina and Brazil, Uruguay’s bordering countries, have reported their last FMD cases in 2006, and according to World Organization for Animal Health (OIE), they have free zones with vaccination and free zones without vaccination. Similarly, the idea is that territories in South America would move from FMD-free with vaccination to FMD-free without vaccination, as evidence of the total eradication of FMD (PHEFA, 2020). This process is one of the specific objectives of the Action Plan 2021-2025 of the Hemispheric Plan for the Eradication of FMD (PHEFA). For Uruguay, this transition might indicate a significant increase in exports prices, and eliminate costs related to vaccination, which were 12 million USD in 2020 (Uruguay, 2019 November 19).
Knowledge on the perception and opinions of veterinarians on large animal disease control programs would help with the discussion of suspending FMD vaccination and the advance towards a new stage of PHEFA. Therefore, our objective was to determine the perception of veterinarians involved in disease control programs (accredited veterinarians) on a future FMD control stage without vaccination in Uruguay.
Materials and methods
Description of the study population
The target population of this survey were veterinarians working in Uruguay who are accredited by the Ministry of Livestock, Agriculture and Fisheries to participate in disease control programs in large animals. The sampling frame of this study was obtained through collaborations with the Ministry of Livestock, Agriculture and Fisheries, who provided a list of all veterinarians accredited as of June 2018. Two strata were determined based on the year of admission to the only Faculty of Veterinary Medicine in Uruguay: “Stratum 1” (pre-FMD outbreak) consisted of veterinarians admitted before or in 2001 and “Stratum 2” (post-FMD outbreak) consisted of veterinarians admitted after 2001. These strata were established in order to investigate whether the fact of having been trained in the veterinary profession in a country with or without FMD, influenced the perception of veterinarians about FMD control practices. The total number of veterinarians in the population was 1134, 708 (Stratum 1) and 426 (Stratum 2).
Sample size
The sample size calculations were performed in order to estimate the true proportion of individuals willing to stop FMD vaccination. Based on previous results (Piaggio et al., April, 2016), this proportion was 23%. Considering a precision of 5%, a confidence level of 95%, and a population of 1134 veterinarians, a sample size of 273 (n=220 adjusted for population size). A stratified random sample strategy was used and to accomplish with the minimum sample size estimated by each Stratum of 110 veterinarians. To take in consideration rejection to participate, 162 veterinarians were randomly selected on each Stratum.
Survey design
1) demographic and professional
information, 2) 10 closed questions regarding the perception on FMD risk, and opinion of the control and eradication measures applied in Uruguay, and
3) specific questions about vaccination and the cost/benefit of an eventual suspension of vaccination
Uruguay was divided into three regions (West, Northeast and Center-South) due to geographical characteristics and production systems, the areas are presented in Fig. 1.
The questionnaire and their possible answers are depicted in Annexed 1. During the questionnaire design stage, a test form was used and the survey was carried out with 10 professors at the Faculty of Veterinary Medicine to assess the quality of the tool. This test form was distributed by email to this test group and the disagreements were discussed between the researchers.
Survey delivery
To carry out the survey, an electronic form was used on Google Forms platform. From August 6th to September 30th of 2018, the link was distributed via e-mail to the Veterinarians selected in the sample. Follow-up emails were sent 6 times. Those veterinarians who did not reply to the email, were contacted via telephone up to 3 times before being considered as non-responders.
Statistical analysis
The stratified study design was accounted by using the relative weight of the individuals in each Stratum using Stata version 12 (College Station, USA) stratified analysis. The probability of selection of an individual was 162/708 and 162/426 for strata 1 and 2, respectively. The inverse of the selection probability was used to weight each individual in the total data analysis. The data were analyzed descriptively for each question, and a logistic regression was used to determine the association between questionnaire variables and willingness to stop vaccination.
The yes category from willingness to stop vaccination was divided in two parts, yes with no conditions, and yes under certain circumstances (which were described descriptively). For the logistic regression, however, the willingness to stop vaccination was restricted to yes vs. no. A univariate logistic regression analysis was used to evaluate the association between demographic and FMD-risk-related questions with willingness to stop FMD vaccination (no vs. yes). Those that indicated not to have an opinion were excluded from the analysis. Those variables that presented a P-value lower than 0.20, and their first term interactions were selected for a multivariable model. The selection of the multivariable model was carried out by means of a backward elimination using a cut-off P-value of 0.05. The final model was determined when all the variables that remained in the model were significant at a P-value less than 0.05.
Results and discussion
Data and scope of the survey
Of the total 324 veterinarians randomly selected for participation in the survey, 256 actually responded the survey (79% response rate). Of the 256 veterinarians that agreed to participate: 48.8% (n1= 125) were from Stratum 1 (pre-FMD outbreak), and 51.2% (n2=129) were from Stratum 2 (post-FMD outbreak). The total percentage of non-response was 20.9% (22.8% and 19.1% first and second stratum, respectively).
Sample description
Descriptive statistics relating to the surveyed individuals and their responses are depicted in Table 1. The mean year of starting to study in the Faculty of Veterinary Medicine was 1991 in Stratum 1 and 2007 in Stratum 2. Most veterinarians, in both strata, reported working with beef (Table 1). However, most of them (61%), worked on more than one animal species, with 21% only working with beef cattle.
Table 1: Descriptive means/percentage (SD) from the two strata defined in our population
a Veterinarians who enrolled in the Faculty of Veterinary Medicine before or in 2001 (pre-FMD outbreak). b Veterinarians who enrolled in the Faculty of Veterinary Medicine after 2001 (post-FMD outbreak c Veterinarians can work on more than one area. d Number of farms where the veterinarian works
Description of the opinion of accredited veterinarians regarding disease control programs on FMD
Veterinarians’ answers regarding FMD risk perceptions are depicted on Table 2 and Fig. 2. Of all surveyed veterinarians only 32.2% had been exposed to FMD in the field (Table 2). In Stratum 1, most veterinarians would score themselves and other veterinarians as a 3 or 4 out of 4 (higher) in their capabilities of diagnosing an FMD clinical case (Fig. 2). However, when asked about other veterinarian’s capabilities, these scores were primarily 2 and 3 out of 4 (Fig. 2). Similar results were observed on Stratum 2 veterinarians (Fig. 2). Most veterinarians on both strata considered there was a low or moderate risk of introduction of FMD in Uruguay (Fig. 2). However, when answering regarding the eradication plan in the region, the most common answer was “no answer” 41.3% (Fig. 2). Most veterinarians (>80% in each Stratum) indicated that vaccination was the most important measure to prevent FMD in Uruguay (Fig. 2). Conversely, more than 50% of veterinarians in each Stratum saw the cost/benefit ratio of stopping vaccination as neutral or inadequate (Fig. 2).
Table 2: Percentage and SE of answers to FMD related questions from a survey of 256 veterinarians regarding FMD control measures, adjusted for sampling strategy
a Veterinarians who enrolled in the Faculty of Veterinary Medicine before or in 2001 (pre-FMD outbreak). b Veterinarians who enrolled in the Faculty of Veterinary Medicine after 2001 (post-FMD outbreak).
Opinions regarding stopping FMD vaccination-multivariable logistic regression
The results from the unconditional associations are depicted in Annexed 2. The probability of being inclined to stop vaccination was 41.7% (n=52) on Stratum 1 and 29.4% (n=38) on Stratum 2, after adjusting for region and the perception of the risk of introduction (Table 3). The region with the highest observed probability of being inclined to stop vaccination was the "Northeast" region (46.3%), followed by “Central-South” (39.2%), and the “West” region (25.3%) (Table 3).
While adjusting for strata and geographic area, veterinarians who considered the risk of reintroduction of the disease in Uruguay was “low,” had a higher probability of being willing to stop vaccination than those in the moderate and high groups (Table 3).
Table 3: Multivariable analysis of willingness to stopping vaccination for FMD in Uruguay among accredited veterinarians
a Veterinarians who enrolled in the Faculty of Veterinary Medicine before or in 2001 (pre-FMD outbreak). b Veterinarians who enrolled in the Faculty of Veterinary Medicine after 2001 (post-FMD outbreak). When looking at the conditions under which veterinarians would be more likely to suspend vaccination, the most common circumstances were: larger epidemiological surveillance (63.2%), border controls (61.8%), and a better regional situation (59.2%) (Table 4).
Discussion
This study is the second study to understand the opinion of accredited veterinarians on vaccination implementation strategies in Uruguay. With 29.4% to 41.7% of the accredited veterinarians being in agreement to stop FMD vaccination under certain circumstances, depending on the Stratum in which they were included, there are still challenges to support stopping vaccination as outlined in the PHEFA.
Our study presented a high response rate (79%), which was comparable to Piaggio’s study (Piaggio et al., April, 2016). This high response rate may be due to the survey delivery method (email and telephone), survey length (short survey), and the generally strong interest in FMD control strategies. Another investigation with similar characteristics to our work obtained a response rate of 31.6% (Caffarena et al., 2018). However, they only used an electronic form, without any other form of follow-up (phone) to contact the non-respondent veterinarians. Our response rate is comparable with that reported by others (Fincham, 2008), who established 70% as the lower limit for response rates on multimodal survey approaches.
The surveyed veterinarians mostly placed their and their colleague’s capability of diagnosing a clinical case of FMD at the highest levels of the scale in the survey. Although there was a slight difference between veterinarian´s self-assessment and their assessment of their colleagues, this difference can be attributed to cultural traditions. Their capacity to clinically diagnose a case is of great importance considering that these veterinarians are in the first line to detect the disease, and a rapid control of a potential FMD introduction will depend on their clinical capacity. This result is comparable to that obtained by others (Piaggio et al., April, 2016), who reported that 64% of their respondents believe that veterinarians are prepared to recognize a clinical case of FMD.
The perception of risk of introduction of FMD in Uruguay in this study is comparable to that obtained by Piaggio’s study (Piaggio et al., April, 2016), which is important given that veterinarians might consider FMD among potential differential diagnosis. Interestingly, even though their perception of risk is close to 40%, more than 60% reported to be concerned of a potential introduction, which might indicate a conservative approach to risk perception.
Although opinions regarding stopping vaccination varied by strata, 41.3% of all veterinarians did not answer whether the eradication/control plan is being carried out correctly in the region. This result could indicate that there is little knowledge about the government’s perspectives and projections of FMD in the region. Given that a high percentage of veterinarians still think that the risk of introduction is moderate, these results on veterinarian’s awareness on regional eradication plans are key in future communication campaigns regarding the disease control efforts. Public awareness and trust in government efforts will be fundamental when facing off the use of vaccines.
Similarly, most veterinarians (>80% in each Stratum) indicated that vaccination was the most important measure to prevent FMD in Uruguay. These results were supported by more than 50% of veterinarians in each Stratum indicating that the cost/benefit of stopping vaccination was neutral or inadequate. The fact that most veterinarians see this ratio as inadequate or neutral might indicate a lack of knowledge on the economic advantages of stopping routine FMD vaccination.
Veterinarians in Stratum 1 had higher probability to be inclined to suspend FMD vaccination than those in Stratum 2. This difference could potentially be explained due to Stratum 1 veterinarians having experienced different FMD control stages (outbreaks, free with vaccination, and free without vaccination). Our results related to willingness to stop vaccination were similar to that obtained by others (Piaggio et al., April, 2016), who reported that 23% of their respondents would be willing to stop vaccination. The study population of Piaggio (April, 2016) only included “post-FMD outbreak” veterinarians (our Stratum 2). Therefore, we can indicate two things, first that veterinarians “post-FMD outbreak” have been consistent in their willingness to stop vaccination, and that their intention is lower than that of veterinarians from Stratum 1.
The highest probability of being inclined to suspend vaccination (46.3%) was found in the Northeast region, which could be explained by the area without vaccination in the states of Rio Grande do Sul and Santa Catarina. This area might act “sentinel” zone (Baigorria, 2012), and provide veterinarians with a certain perceived protection. The West region reported the lowest probability of being inclined to suspend vaccination (25.3%), which could be related to the area in which the last FMD cases were introduced in 2001.
Although our study sampling strategy had the advantage of using a national registry for accredited veterinarians as a sampling frame, this does not include those non-accredited veterinarians. National surveillance activities comprise a large source of revenue to livestock veterinarians, and most veterinarians would be registered as accredited veterinarians in order to access that source of income. Thus, we did not consider this to be a large source of selection bias. Although there was a high response rate, no evaluation of demographic characteristics by respondents and non-respondents was carried out, which could have helped to identify potential selection bias.
Conclusion
Veterinarians who enrolled in the Faculty Veterinary Medicine before or in 2001 (Stratum 1) were more likely to be willing to suspend vaccination than those in Stratum 2. The area of residence and professional activity was associated with different opinions towards vaccination. These results highlight the perception of veterinarians regarding FMD control practices in Uruguay. Although large efforts have been put in place to eradicate and prevent FMD outbreaks, Uruguay’s veterinarians still rely on the use of vaccination to control FMD. The knowledge produced through this survey will aid on the decision making process of the official veterinary services on future FMD control programs.
