What if a Bioterrorist Attack Occurs?—A Survey on Citizen Preparedness in Aveiro, Portugal

Abstract

Introduction: A bioterrorist attack is the intentional release of pathogenic micro-organisms, such as viruses, bacteria, or their toxins, with the aim of causing illness or death in people, animals, or plants. In this study, we investigated the knowledge and practices related to bioterrorism preparedness in Central Portugal. Methods: A descriptive cross-sectional study was performed with a convenience sample in the population of Aveiro, Central Portugal, to assess their knowledge about bioterrorism, self-perceived preparation to act in case of bioterrorism and pet owners’ preparation. An online validated questionnaire was completed by 198 participants from January to February 2020. Results: In this study, 46.0% of the respondents answered that they knew nothing about bioterrorism or had never heard about the possibility of bioterrorist attacks. In the case of an attack, 77.8% participants did not consider themselves prepared to act, and 62.1% did not know how to use personal protective equipment. More than half of the respondents (60.6%) were not familiar with the local emergency response system in response to catastrophes/bioterrorist attacks. Almost all respondents (95.6%) assigned high importance to drinking water and food for pets, but only 22.9% of respondents attributed high importance to pet carrier boxes, an item essential for cat evacuation. Conclusion: This is the first survey of this kind in Portugal concerning bioterrorism preparedness in citizens and animals. Results suggest that Portuguese knowledge is limited, and people have inadequate preparedness for a bioterrorist attack. These results reinforce the importance of further studies to better understand the existing gaps in knowledge of Portuguese citizens, strengthen the need to adopt the One Health concept in preparedness plans and emphasize the crucial role of health education in prevention.

1. Introduction

Bioterrorism refers to a intentional release of micro-organisms—namely, bacteria, viruses, or toxins—whose purpose is to cause morbidity or mortality to as many individuals as possible, be they humans, animals or plants [1]. There has been a growing interest in the use of biological agents as weapons by terrorist groups, with several having already explored their use on a small or large scale [2]. The impact of such attacks has the potential to be high, as their intention is to generate victims, terror and social disorder, or economic losses due to ideological, religious or political reasons [3,4].

Previous studies have shown that the number of victims can be reduced by about 75% with proper prior preparation. This encompasses several areas, including the enrichment of public health in the diagnostic, surveillance, therapeutic and community education sectors. This approach will be conducive to lower economic costs, compared to those of a nation whose risks of bioterrorist attacks have not been properly addressed [5,6].

Lack of attention to disaster warnings might lead to considerable damage, which suggests a need to pay attention to bioterrorism prevention and preparedness [7]. Knowledge of owners’ preparedness for disasters and emergencies is crucial in effective disaster management [8,9]. This approach emphasizes the important roles and responsibilities of the members of the community [10]. However, studies on bioterrorism preparedness, public knowledge and risk perception are scarce [4,11,12,13,14].

It is therefore of paramount importance to promote and educate citizens to effectively respond to bioterrorism, and to increase their awareness and preparation for potential bioterrorist attacks and of how they can be initiated, infection control, timely communication of occurrences, biosecurity and collaboration with authorities [15,16]. This study aims to strengthen the value of combating the impact of potential bioterrorist attacks by promoting preparedness among the general public and pet owners, underlining the importance of knowledge and self-perception of the need for training.

2. Materials and Methods

A cross-sectional study to assess knowledge about bioterrorism, self-perceived preparation to act in case of bioterrorism and pet owners’ preparedness was conducted from January to September 2020. A voluntary survey was carried out among a convenience sample of 198 participants from the municipality of Aveiro, a popular tourist destination near the sea with 80,880 citizens in Central Portugal, similar to other Portuguese cities (Figure 1), which is a medium-sized country on the European scale [17].

Individuals were eligible to participate if they were at least 18 years of age. After agreeing to participate in the study, each participant was asked to complete an anonymous, confidential 15 min self-administered written questionnaire distributed on online social media platforms. The sample size of this study was calculated according to a formula for survey sample sizes [18].

Assuming a 10% default prevalence (based on the reviewed relevant articles), a 95% confidence level and a 10% absolute error, 155 participants were required for the study. To allow for a 10% non-response, the smallest sample size required was 198 participants.

The questionnaire was based on a literature review [19,20,21,22,23], and designed by the authors (veterinarians and epidemiologists) to obtain information about bioterrorism preparedness. The questionnaire consisted of closed and short-answer questions (which could be categorized) and was previously pre-tested to improve validity and reliability. Thereafter, it was applied to 55 non-participants in the district of Vila Real (North Portugal) before the study was initiated to help improve the clarity of the questions and ensure that the estimated time needed to complete the survey (approximately 15 min) was adequate.

The questionnaire consisted of 37 questions and collected the following information: demographic characterization of individuals (gender, age, marital status, education level, number of children under 12 years of age in the household and presence of pets and other animals). Knowledge regarding bioterrorism (self-perceived by the participants in relation to protecting themselves), ability to act in a bioterrorist attack situation and in the face of the possible occurrence of a bioterrorist attack, and questions to pet owners about animal protection were also addressed. In the questions with closed-ended responses on the importance of items associated with pets in a bioterrorism situation, a 6-point scale answer ranked from 0 to 5 (0 = not important; 1 = very slightly important; 2 = slightly important; 3 = important; 4 = very important; 5 = extremely important) was used.

The study received ethical approval from the Ethics Commission of the University of Trás-os-Montes e Alto Douro (Doc91-CE-UTAD-2019).

Data Analysis

Data were entered into an Excel database (Microsoft Corporation, Redmond, WA, USA) and exported and analyzed using SPSS version 25.0 (SPSS, IBM Corporation, New York, NY, USA). For descriptive purposes, the Pearson χ2 test was conducted for each variable in the study, looking at sociodemographic differences. Statistical significance was based on a p-value < 0.05.

3. Results

Regarding gender, 65.2% (n = 129) of respondents were women and 34.8% (n = 69) were men. In relation to academic background, 74.7% had secondary or higher education (completed or attended). As for marital status, 42.9% (n = 85) were married or lived as an unmarried couple. About 30% (i.e., 29.8%; n = 59) of the respondents lived with children under 12 years. Pets were owned by 67.7% of respondents (134/198), mainly dogs or cats. About 27% (i.e., 26.8%; n = 53/198) of the respondents had pets of different species.

3.1. Knowledge Attitudes and Practices of the Population regarding Bioterrorism

In this study, 46.0% (n = 91) of the respondents did not know about or had never heard of bioterrorist attacks. About 28% (i.e., 28.3%; n = 156) of respondents had never thought about this possibility. Regarding sources where respondents could find information about bioterrorist attacks and how to act against them, 49.5% (n = 98) had never thought about it, and only 16.2% (n = 32) reported knowing where they could find information. Most respondents (i.e., 91.4%; n = 181) did not read newspaper or magazine articles related to preparing to act in the event of a bioterrorist attack. Almost three-quarters of respondents (74.2%; n = 147) considered the lack of information as an obstacle to their degree of preparedness. Of the respondents, 69.7% (n = 138) reported that they did not regularly perform accident/emergency drills at their workplace. When accident/emergency drills were performed, they were normally about fire. Participants were asked if they had held seminars or lectures in the workplace in the context of bioterrorism, and 78.8% (n = 156) replied no. However, 72.7% (n = 144) of the respondents considered that seminars or lectures on how to act in the face of a bioterrorist attack would be important. About 63% (i.e., 63.1%; n = 125) of respondents revealed an interest in participating or attending these lectures in the future. Respondents were asked about their knowledge of infectious diseases that could be caused by a bioterrorist attack. To this question, 80.3% (n = 159) of the respondents answered that they did not know of any infectious diseases. Among those who knew of some diseases, the following were mentioned: anthrax (n = 10), smallpox (n = 8), Ebola (n = 3), foot-and-mouth disease (n = 2), influenza A (n = 1), cholera (n = 1), viral diseases (n = 1), any bacterial and viral etiology (n = 1), allergies (n = 1) and poliomyelitis (n = 1). Among those who responded that they were aware of infectious agents that could cause a bioterrorist attack, 9.6% of respondents (n = 19) claimed to know some typical clinical signs. The clinical signs reported by respondents were rash (n = 7), fever (n = 7), respiratory problems (n = 6), headache (n = 5), vomiting (n = 4), diarrhea (n = 4), muscle pain (n = 3), fatigue (n = 2), abdominal pain (n = 2) and bleeding (n = 2). No sociodemographic characteristic under study was statistically associated with questions about bioterrorism variables. Figure 2 presents a summary of the answers given to the questions about bioterrorism.

3.2. Knowledge Attitudes and Practices of the Population about Bioterrorism Preparedness

With regard to bioterrorism preparedness in the case of an attack, most respondents (77.8%; n = 154) did not consider themselves prepared to act and did not know how to use personal protective equipment (62.1%; n = 123). Of the respondents, 26.8% (n = 53) reported a complete lack of preparedness or total absence of preparedness for a bioterrorist attack. Regarding a decontamination plan, most respondents did not know how to act (61.1%; n = 121) and 31.8% (n = 63) reported a total lack of knowledge. Respondents were asked if they had participated in any planning preparedness, and 83.3% (n = 165) responded negatively. Participants were also asked if they considered there was sufficient support from governmental entities in the case of a bioterrorist attack. To this question, 41.9% (n = 83) considered that there was insufficient support, and 53.5% (n = 106) had never thought about it. Most respondents did not know whom to contact in the event of an attack (83.3%; n = 165). More than three-quarters of respondents (i.e., 76.3%; n = 151) did not have a list of contacts for entities that they could call in case of disaster/bioterrorist attack. Almost all respondents (i.e., 94.4%; n = 187) did not know the local protection plans or the places that would receive their family or pets in a disaster/bioterrorist attack. Likewise, almost all individuals, i.e., 97% (n = 192), did not have a family emergency plan in case of a disaster/bioterrorist attack. In the event of a bioterrorist attack, 52.0% (n = 103) of the respondents thought that their pet would stay with them. Respondents were asked if they had an emergency kit in their home consisting of food and water supplies, first aid, medication, medical records, or other items that would allow their family to subsist for at least 7 days, if necessary. Most respondents answered negatively (i.e., 88.4%; n = 175).

Respondents were asked if they had an emergency kit for pets consisting of food and water supply, first aid, medication, medical records, or other items that would allow their pets to survive for at least 7 days if isolation or evacuation was ordered. To this question, only 9.6% (n = 19) of the respondents answered affirmatively. Participants were asked if they considered that their pets were socialized with people and other animals. To this question, 16.2% (n = 32) of the respondents answered affirmatively. As for carrier boxes, 28.8% (n = 57) of the respondents answered that their animals had not been trained for them. In this study, 86.4% (n = 171) of respondents considered that it was important to socialize the animals and train them with leashes or carrier boxes. Women answered affirmatively more often to both questions compared to men. These differences were statistically significant (p = 0.018) regarding both questions. In this study, 34.8% (n = 69) of the respondents stated that their pets had a microchip, and 91.9% (n = 182) attributed importance to pets’ electronic identification. Apart from gender difference on the importance of socializing pets and training them for the carrier box, no other bioterrorism preparedness variable was statistically associated with demographic characterization variables. The summary of responses is presented in Figure 3.

3.3. Level of Importance Attributed to Items in an Emergency Pet Disaster Preparedness Kit

Respondents were asked about the level of importance of items in an emergency pet disaster preparedness kit on a 6-point scale ranging from 0 (not important) to 5 (very important). The results are shown in Figure 4. All items in the list were considered indispensable for animals in a pet disaster situation. However, it was not explained to respondents that all items were constituents of the kit according to the CDC [22]. A great majority (i.e., 95.6%) attributed high importance to a 1–2-week supply of pet food and drinking water (a score of 5 out of 5). As for the importance given to food and water bowls, around two-thirds (i.e., 65.1%) attributed high importance to these items (scores 4 and 5). Regarding the item “pet toys”, 47.5% of respondents did not assign it any importance (score 0) and 41.0% assigned it low importance (scores 1 and 2). Regarding first-aid kits, a majority of more than two-thirds (i.e., 70.5%) attributed high importance (score 5 out of 5). Regarding veterinary records, medical instructions and animal feeding instructions, about 38.9% of the respondents attributed high importance to these items (score 5). Regarding cleaning supplies (plastic bags and litter boxes, in the case of cats), only 31.3% attributed high importance to these items (score 5). As for the carrier boxes, 31.3% attributed a score of 3. It should be noted that 5.5% of respondents did not assign any importance to this item (score 0). Only one quarter of respondents (25.3%) attributed high importance to blankets (score 5). As for leashes and collars, 45.9% attributed high importance (scores 4 and 5). It should be noted that 17.8% of respondents did not assign any importance to these items (scores 0 and 1).

4. Discussion

To the best of our knowledge, this is the first study examining the knowledge and practices about bioterrorism preparedness in a Portuguese population. Knowledge, correct attitudes and practices are the most effective strategies to mitigate adverse effects [24].

This study showed gaps in knowledge about bioterrorism. Indeed, society in general is largely unprepared, despite its civil obligation to understand these issues and formulate opinions. One of the consequences of this lack of knowledge is that superior decision-making is carried out without feedback from the community, which precludes action based on interests, resulting in measures that are inadequate for the community [25].

In the present study, only 16.2% of respondents reported knowing where to find information on bioterrorism, and the vast majority did not read articles or magazines on the subject. About three-quarters of the population considered the lack of information as an obstacle to their preparation for this situation. To mitigate a disaster, health literacy is important, as it provides the community with timely information about the threat and the actions recommended by governmental organizations (defining the threat, explaining its consequences and what can and is being done to minimize them) [26]. Bioterrorist attacks introduce unknown factors through their invisibility and prolonged duration and, consequently, fear. The ability to read, understand and use information could enable people to improve resiliency and reduce disaster risk [27]. Public views about bioterrorism indicate that emergency response agencies must consider public preferences and attitudes that are contingent on pre-existing biases rather than simply on the science of hazard mitigation, and that these may be subject to local attitudes toward government [28]. Other studies about bioterrorism and local agency preparedness have found that information related to bioterrorism responses should be provided to agencies that do not normally work in public health but that would be involved in responding to a biological agent event [29].

In the professional environment, most respondents mentioned that their workplace had not carried out regular emergency drills or training in the field of bioterrorism, although most respondents mentioned an interest in participating in training.

As for self-perceived preparation to act in cases of bioterrorist attacks, the majority said they did not consider themselves prepared to act, and they did not know how to use personal protective equipment or perform the biological decontamination of humans or animals. This is a worrying situation, since in the face of an unknown situation, people who are unaware of a danger tend to act in the most reasonable way to reduce it, which may not always be the most correct or innocuous one. Thus, it is important that actions are recommended by official entities; otherwise, in addition to acting inappropriately, the community can easily panic [26].

Most respondents reported never having participated in planning actions and were unaware of civil protection plans. In the case of a bioterrorist attack, the community expects the government to provide protection and guidelines for action [30,31]. In the absence of effective response plans, the population, in addition to inappropriate attitudes, will lose confidence in higher entities, failing to comply with the measures imposed and endangering their safety and that of others [26].

Concerning the preparedness of pet owners, their lack of preparation is an identified risk factor associated with failure to manage emergencies or disasters [32]. If home evacuation becomes necessary, more than half of the respondents considered that their pets would remain with them. As has already been observed in several situations, the human–animal relationship is something that cannot be disregarded to guarantee the success of evacuations. As in previous situations (e.g., during the evacuation of humans because of Hurricane Katrina), thousands of people refused to leave their homes because their animals were not included in the evacuation plans, resulting in countless human and animal victims. Of the animals that were rescued, only a small number were reunited with their owners [33]. It is therefore important that pet owners are informed that their animals must be evacuated to a place other than human shelters due to health and safety considerations. Many victims may refuse to put their animals in a shelter if they are not sure that their animals will be well taken care of [34]. Information/education is the most powerful tool to save as many individuals as possible, informing them of where their animals are going and their conditions and how they can increase the success of a future meeting (e.g., through identification of their animal).

About 80% of respondents reported not knowing who to contact in the event of a bioterrorist attack, and more than three-quarters did not have a list of contacts to turn to in these situations. Likewise, more than 80% reported not having a family emergency plan or an emergency kit for their family at home. Only 9.6% reported having an emergency kit for their animals. According to a study by Heath et al. [35], in a flood situation in California, about half of the target households reported having no emergency plan in the event of a disaster, particularly for a potential evacuation, either for their relatives or their pets. About a third of the animals were not evacuated in this event, as their owners did not know how to catch or transport them, or where to take them.

About half of pet owners reported that their animals had a microchip, but 91.9% considered this type of electronic identification to be important. There is still a long way to go in Portugal in terms of pet identification, namely in the education of owners of their importance, which in this case is related to an increased probability of animals being reunited with their owners. A previous study performed in Portugal showed that microchipping and municipal registration are often overlooked in the country [36]. Heath et al. [35] demonstrated that the abandonment and failures in the evacuation of pets reflected decreased levels of care for them, namely in the absence of personal identification.

As for the behavior of the animals, only 16.2% of the respondents reported that they were socialized and 28.8% were trained to use a carrier, although 86.4% considered socialization and training for the carrier important. In a study by Heath et al. [35], about a third of households did not evacuate their pets because they were unable to transport them or because they could not be captured, and dogs that were kept mostly outdoors were at greater risk of failing evacuation due to the difficulty in catching, transporting, or even housing them. If dogs are not socialized to live with people when young, human contact can cause them a considerable amount of stress and fear. This can appear as extreme agitation and aggression or even paralysis [37].

In the present study, the level of importance that pet owners attributed to the components of an emergency pet bioterrorism disaster preparedness kit was also studied. A list was given to pet owners. All items provided were considered indispensable for pets in a disaster situation as a bioterrorism situation [22,38,39].

Almost all respondents (i.e., 95.6%) attributed high importance to drinking water and food. As this is a fundamental asset for ensuring animal health and survival, as in a disaster the storage of food and drinking water may be unavailable for sale for a few days, it is considered that owners were aware of the importance of this topic.

Regarding the importance attributed to water and food containers, 38.6% attributed high importance to them. The existence of water and food containers facilitates meal times, keeps water ad libitum, and allows animals to be fed more hygienically. These are important items, as animals, particularly dogs, have a hard time drinking from suspended sources (such as from slanted bottles). This could be because the ingestion of water in dogs and cats is carried out through the adhesion of the liquid to the dorsal surface of the tongue when it penetrates the water in the container, and which is then trapped between the wrinkles of the palate and the back of the tongue, so that it remains in the oral cavity and is then ingested [40].

Regarding item “pet toys”, only 1.5% of respondents attributed it with high importance. A study in the Netherlands found that the use of chewable toys by dogs in kennels stimulated their appetitive behavior and increased their level of physical activity, and decreased their stress levels, at least in the short term, thus promoting the welfare of dogs housed in kennels [41,42]. Regarding cats, it is important to understand that playful behavior is natural in all cats, being a release of energy and stress that can help felines adapt to a new environment in a rescue shelter [43]. In the present study, the utility of toys was neglected by owners, most likely due to a lack of knowledge about the consequences of stress on animals. Stress-inducing events, such as an evacuation and having to stay in new individual housing, but in the same space as many other animals, can result in social and spatial isolation; insufficient physical exercise, environmental stimulation, or human attention; or even fear, which can lead to injuries arising from fight-or-flight responses. If prolonged in time or very frequent, they can also lead to chronic stress, leading to an increase in anxiety, inhibition of normal behaviors and a decrease in immunocompetence [44]. Play can be a way for dogs to reduce anxiety and fear and improve well-being. On the other hand, fear in dogs is a cause of aggression, so the presence of a known and appreciated toy can be equally beneficial in preventing aggression [45,46].

As for a first-aid kit, 70.5% of the respondents attributed it with the highest importance. This is also an interesting value, as this item can be very valuable both in evacuation situations, where animals can get sick or in some way injured, or in the event of staying at home, for the same reasons [47].

Regarding the item “veterinary records, medical instructions, feeding instructions”, 38.9% of respondents assigned these great importance. In a disaster, it is important to keep animal documents, especially copies of medical and vaccination records, animal photos, and 2 weeks of medication, along with their instructions for administration, with the owners. This will allow owners to check if pet vaccination and deworming is up to date, as well as to save potentially more detailed information about animal health [22]. This is a very important item as, in the event of the existence of such a disease or condition, the failure to administer daily medication or the administration of inappropriate therapy can threaten the animals’ lives.

Regarding cleaning supplies (bio-hazard waste bags, paper towels, plastic bags), 31.3% of respondents attributed great importance to these. It is known that the urine of animals (and humans) contains ammonia in amounts that, if inhaled continuously, can lead to the development of respiratory diseases and skin and eye irritation. Dog and cat feces contribute to the development of bacteria, viruses, and parasites, which can ultimately cause disease in humans or animals [48]. Added to this is the discomfort caused by the intense smell that waste can have. Thus, these hygiene items are very important for the maintenance of animal and human well-being and public health.

In the present study, 25.3% of respondents gave high importance to blankets. In fact, in a bioterrorism situation, this item is important because hypothermia may occur due to exposure to cold air, especially in the cases of wet fur or soaking in cold water for a long period of time [49]. A prolonged hypothermia situation can lead to the death of the animal, with a blanket being extremely important as a preventative measure [50]. As for blankets, they are important not only for providing comfort to the animal, especially if they are far from owners, but also for preventing hypothermia situations in cases when it is necessary to evacuate to other places, if they are cold or if there is shortage of material. Another function that can be considered is the possible assistance in the containment of animals in case it is necessary to carry out certain veterinary or medical procedures, or even for transportation purposes.

Regarding carrier boxes, 22.9% of respondents attributed high importance to the item. According to analyses carried out in a study by Heath et al. [35], a higher prevalence was associated with the unsuccessful evacuation of cats in households that did not have transport boxes. Furthermore, these boxes allow cats to exhibit concealment behaviors, which can help reduce their stress by allowing a normal feline coping mechanism [51]. Kry and Casey [52] showed that providing a hiding place improves the well-being of cats entering a new or stressful environment by allowing them to display their natural behaviors and reducing stress, which leads them to demonstrate less aggressive behaviors towards humans. Previous studies have shown that owning insufficient carrier boxes has been identified as a important impediment to pet evacuation particularly for feline evacuation [53,54]. Carrier boxes are important not only for the ease of transport of cats but also of small dogs. In addition, a study in the Netherlands on cats housed in animal shelters found that having a box where they could hide was responsible for reducing cat stress, at least in the short term [55]. Similarly, regarding leashes, collars, and tags, 23.8% respondents attributed high importance to these items.

There must be communication and action plans that combine the fields of veterinary medicine, military defense, public health and information services in the formation and application of the law. Consequently, it is important to establish organizations, preferably in all counties, with public health veterinarians, to facilitate intersectoral communication and improve the surveillance system. Another important measure would be their continuous training in the knowledge, prevention and control of emerging diseases. In addition, the elaboration of adequate legislation and the provision of financial assistance for laboratory equipment are both necessary [56].

It is necessary to analyze the current legislation and evaluate the measures to prevent terrorist activity. The main function of legislation should be to prepare the country and its inhabitants to minimize the harmful effects of a terrorist attack through prevention in various sectors, such as veterinary medicine, public health, the Armed Forces, politics, communications, logistics and agriculture, among others, and the proper management of the response [16,57].

This study reveals several gaps that may need to be filled associated with health education in the bioterrorism of the community and its animals.

5. Study Limitations

The limitations and potential sources of bias in this study must be considered when weighing the results. This survey may have not adequately targeted the population, since the sample was a convenience sample from the metropolitan region of Aveiro. Since the survey was administered via social media, it could skew towards younger people, with a high self-selection factor. A third limitation is the self-reported nature of this study and its cross-sectional assessment. Therefore, studies should be conducted in other cities of the country to characterize geographical and cultural differences.

6. Conclusions

In this study, nearly half of the respondents had never thought that a bioterrorist attack would happen, and the results suggest that the community is unprepared. Based on our findings, we suggest that the government should conduct educational activities and make updated information available for the population through multiple easy-to-follow forms. County-level organizations and veterinary medical centers, among others, should collaborate with veterinary public health authorities to increase knowledge and eliminate behavior gaps, and improve pet owners’ preparedness. Despite some limitations, this survey could be a useful tool for decision makers to promote programs and campaigns aimed at informing about bioterrorism preparedness.