Preventing Australian Bat Lyssavirus: Community Knowledge and Risk Perception of Bats in South East Queensland

Introduction

Bats are implicated in the transmission of a range of viruses around the world including rabies, Nipah, Hendra, and most notably in Australia, Australian bat lyssavirus (ABLV) (Calisher et al. 2006). Bats may directly transmit ABLV if they are infectious and bite or scratch a human (Calisher et al. 2006).

ABLV is closely related to rabies virus, and human infection resembles classical rabies (Moore et al. 2010). Although Australia is otherwise rabies free, to date, there have been three fatal human cases of ABLV, all in the state of Queensland (Allworth et al. 1996, Hanna et al. 2000, CDNA 2012, brisbanetimes.com.au 2013). The first case prompted recognition of ABLV as a disease of public health importance, with guidelines for prevention first published in 1996 (Hanna et al. 2000). Human cases have been notifiable nationally in Australia since 2001 (Blumer et al. 2003), but potential human exposures (notifiable in certain states including Queensland) are not nationally notifiable (Australian Government Department of Health and Ageing 2004).

Some Australian states have reported on local surveillance of potential exposures over short periods (Torvaldsen and Watson 1998, Fielding and Nayda 2005). Surveillance in South East Queensland has been ongoing and identified 385 notifications of potential exposure between November, 1996, and October, 2008, in a defined geographic area (Young and McCall 2010). Of these, an average of 55% (around 14 people annually) required postexposure prophylaxis between 2000 and 2008. The majority of people potentially exposed (52%) were members of the public who attempted to rescue entrapped bats (Young and McCall 2010).

Public health messages targeting community members in Queensland have been broadcast through local and state media at least annually since the late 1990s and are featured on the state government Department of Health and other websites (Queensland Health 2010, Queensland Health 2011, Queensland Government Department of Agriculture 2012, Australasian Bat Society Inc. and Queensland Government, not dated). The messages warn people not to handle bats, but to call in vaccinated trained handlers if required. Despite these ongoing prevention efforts, notifications of potential exposures have failed to decline since the turn of the century (Young and McCall 2010).

In light of this finding, this cross-sectional community survey aimed to measure the knowledge and risk perception of adults in South East Queensland and investigate reasons why people might handle bats, with the aim of informing future public health campaigns for preventing potential exposures to ABLV.

Participants and Methods

A social marketing company was contracted to administer a purpose-built computer-assisted telephone interview (CATI) survey to 700 adults (aged 18 years or older) from South East Queensland (Fig. 1) in May–June, 2012. Age and gender quotas, based on the 2010 estimated resident population, were applied to ensure the sample was representative in these respects.

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FIG. 1.

Geographic area of survey in South East Queensland, Australia. Color images available online at www.liebertpub.com/vbz

Eligible phone numbers were randomly generated, then subject to validation as household numbers prior to use in the survey. Listed and unlisted numbers, but not mobile phone numbers, were therefore included.

Exclusion criteria were: Residing outside the study geographic area, inability to respond to the telephone survey because of language difficulties, currently working with or handling bats (including flying foxes) whether as a professional or as a volunteer, and having been previously bitten or scratched by a bat. The survey included both discrete-choice and open questions, and asked participants about their perceptions of the risk to human health from bats, whether they would attempt to handle a bat in a variety of situations, their knowledge of bats and disease transmission, and demographic information.

The survey was pilot tested with 39 adult members of the general public, and adjustments made to the wording of some questions to ensure clarity in communication before recruitment proper commenced. A total of 15 interviewers employed by the social marketing company conducted the interviews using the scripted questionnaire. The marketing company used project briefing and ongoing supervision to ensure consistency of interview technique.

Data analysis was performed on SPSS version 19.0, and epiInfo 6.0. Descriptive analysis compared proportions using the chi-squared test.

Twelve knowledge questions were coded: 1=correct answer and 0=incorrect answer or don't know. The responses were summed to give an overall knowledge score, with a higher score indicating more correct answers.

The responses to 10 risk perception questions were coded: 0=no risk, 1=low risk, 2=moderate risk, and 3=high risk. The responses were summed to give a risk perception score. To account for questions where individuals answered “don't know,” each raw score was divided by that individual's highest possible score. The result was a decimal between 0 and 1, with values closer to one indicating greater risk perception regarding bats.

Twelve questions about participants' intention to handle bats in different situations were coded: 0=no intention to handle and 1=intention to handle. The small number of “don't know” responses to these questions (0.9%) was coded as 0.5, given that both 0 and 1 are equally valid in this situation. The responses were summed to give an overall intention to handle bats score. The higher the score, the more situations in which an individual indicated they would handle a bat.

Knowledge, risk perception, and intention to handle scores were categorized, because none of these approximated a normal distribution. Chi-squared tests compared score categories across the range of demographic variables and the relationship of scores to each other. Significant associations with the intention to handle bats were then included in a preliminary multivariate model. Backward, stepwise, multinomial regression was applied with the criteria for removal of factors set at p≥0.05. Handling a bat that has been dead for greater than 4 h does not pose a risk of exposure to ABLV (CDNA 2012), thus we undertook sensitivity analysis by recalculating the overall intention to handle score excluding the scenario involving a dead bat and rerunning univariate and multivariate analyses.

The responses to open questions about reasons for handling or not handling bats and the risks to human health from bats were entered verbatim into the database at the time of interview. We analyzed the responses to these questions thematically. We adopted a realist method of thematic analysis using an inductive approach (Braun and Clarke 2006). We initially coded the text transcripts at the level of the phrase, reviewing the preliminary codes to refine a set of concepts, and then considered the relationships between concepts to encode preliminary themes. We refined these in the context of the entire data set before concluding and reporting the key themes.

The study was approved by the Queensland Health Central Human Research Ethics Committee.

Results

To obtain the sample of 700 adults, 7970 unique phone numbers were called. Of these, 1503 (19%) were ineligible due to age-gender quotas, working with or being previously bitten by a bat, or language barriers; 2522 (32%) were not answered; in 1065 (13%) the eligible person was not able to be contacted; and in 2180 (27%) the eligible person refused participation. The participation rate was: 24% of contacted eligible people (700/2880), 18% of known eligible people (700/3945), and 11% of all possibly eligible people (700/6467).

In accordance with the required quotas, 49% of participants were male, and more than half (53.6%) were aged less than 45 years. Sixty-three percent of participants were employed at the time of the survey. Seven percent had ever worked or volunteered in the animal health industry, and 20% had ever worked or volunteered in the human health services industry. Sixty percent had completed either a technical and further education (TAFE), trade, or university qualification.

The majority of participants felt that bats were a danger to human health, with 20% indicating a high risk, 31% indicating a moderate risk, 42% indicating a low risk, and 4% indicating no risk to human health. Three percent of participants did not have an opinion.

Participants were asked what they thought were the risks to human health from bats. Although participants could not always be specific, disease transmission, including viruses and bacteria, was a key theme. Participants were concerned about diseases transmitted via bat droppings, bites, and scratches. Responses indicated knowledge and concern about Hendra virus more than other diseases, although ABLV and rabies were also frequently mentioned. Participants associated a variety of other viruses and bacteria with bats, including influenza and equine influenza, severe acute respiratory syndrome (SARS), dengue, Listeria, and Salmonella.

Another theme was that participants felt bats' impact on the physical environment was a hazard to human health. The noise and smell of bat colonies were felt to be health risks. Bats eating fruit meant for human consumption was of concern, as were bat droppings around people's homes.

However, the other key theme in these data was uncertainty about the health risks posed by bats. Although people felt there was a risk, they were uncertain what the risk might be, or could recall the name of one or more viruses they associated with bats, but did not know what the virus/es meant for human health.

Of the 700 participants, “lyssavirus” or some variety of this was mentioned by 67 (10%) as a human health risk posed by bats. “Hendra” was mentioned by 207 (30%). However, when asked specifically about ABLV, a further 327 participants (47%) had heard of the virus, and 24 (3%) felt they might have heard of it.

Participants were asked to rate a variety of situations in terms of the risk to human health (Table 1). Bats interacting with people and bats interacting with pets were identified as the most risky scenarios. However, high proportions of people would still personally attempt to handle bats in a variety of situations (Table 2), including these “riskiest” situations. The survey defined “handle” as any type of contact, whether with hands, gloves, or some type of implement. Of relevance to the apparent discrepancy, 27% of participants incorrectly felt that wearing gloves nullified the risk from bat handling, 54% (correctly) thought that not all bats carry lyssavirus, and 11% incorrectly thought that only bats that appear sick are a risk to human health.

Participants were asked if there was any other situation (not specifically named in the previous scenarios) in which they would handle a bat. Fifteen per cent (n=107) indicated there was. These responses were coded. Of these participants 36% (n=39) would handle a bat if the bat was attacking them or a member of their family, and 37% (n=40) would handle the bat if it needed rescuing in other situations. The remainder gave other reasons such as removing the bat from their personal environment.

Eighty-six participants (12%) indicated they would not handle a bat in any situation. When asked why, the key theme was the potential adverse consequences to themselves. The potential transmission of lyssavirus was specifically detailed as a reason not to handle bats, although the fear of “disease” transmission in general was predominant. Either with or without the fear of disease transmission, being bitten or scratched was a particular concern. Concern that handling a bat may damage was a less dominant theme.

The other 624 participants were asked why they would handle a bat in the circumstances they had indicated. A key theme was protection. People either wanted to protect their family, friends, pets, and themselves from the bat, or wanted to protect the bat from harm. Even in situations where the person had indicated they would only handle a dead bat, people frequently felt that they would do so to prevent harm to pets and others, or to maintain the cleanliness of their environment. Children and pets were given priority over personal safety. Similarly, baby bats were sometimes felt to be in need of saving preferentially.

Another key theme was the perception of minimal or no risk. People felt that using an implement, gloves, or a towel when handling a bat would protect them from injury and therefore minimize the risk from handling. This sentiment was applied to a variety of handling situations; for example, as a way of minimizing the risk to self while protecting others, rescuing a bat, or removing a bat from the house. Dead bats were not felt to pose a high risk, and using an implement or gloves during disposal was felt to eliminate any risk to health. In some cases, baby bats were seen to pose less of a risk of injury than adult bats. However, in some of these cases, and more generally there was an overlying theme of handling as a last resort. People expressed the need to act more quickly in some situations than trained handlers could attend the scene.

The final key theme was the perception that handling was necessary, although not emergent. It was felt that to remove a bat from your property, particularly a live bat entering your house or a dead bat in your yard, was required; that not handling was not an option.

When knowledge questions were summed, the median was 9 (possible range 0–12); the interquartile range was 8–10. Overall risk perception had a median of 0.667 (possible range 0–1); the interquartile range was 0.467–0.833. The median for overall intention to handle bats was 4 (possible range 0–12); the interquartile range was 1–6.

On univariate analyses (Table 3), there were a number of demographic associations with knowledge, risk perception, and intention to handle bats. Notably, males were more likely than females to score in the lowest quartile of risk perception and more likely to indicate intention to handle bats. These relationships were unaltered when intention to handle was recalculated after excluding the scenario involving a dead bat.

Knowledge score did not predict risk perception (p=0.065) or intention to handle bats (p=0.310). However, risk perception was associated with overall intention to handle bats (p<0.001). Those in the lowest risk perception quartile were 2.47 times (95% confidence interval [CI] 1.68; 3.62) more likely to score in the highest intention to handle quartile compared to those in the highest risk perception quartile. Again, this relationship was not altered when intention to handle was recalculated after excluding the scenario involving a dead bat.

On multivariate analysis, the final model included gender, age group, and overall risk perception (Table 4). Being male, in a younger age group, and having a lower risk perception of bats increased the likelihood of indicating intent to handle bats in greater numbers of situations. The final model included the same variables and similar odds ratios when intent to handle was recalculated after excluding the scenario involving a dead bat.

Discussion

This cross-sectional telephone survey of community members without previous potential exposure to ABLV indicated high levels of basic knowledge about bats and ABLV, moderately high risk perception of bats in general, and overall low intentions to handle bats. However, the vast majority of participants felt that handling a bat might be necessary in some circumstances to protect themselves or others or to assist a bat in distress. Young adult males with lower risk perceptions of bats indicated more frequently that they would choose to handle a bat in different situations. This finding is consistent with a male predominance in potential exposure notifications from the general public in recent years (Young and McCall 2010). Using gloves or implements was often felt by survey participants to reduce or nullify any risk of injury from handling bats. Liesener et al. (2006) surveyed by telephone community members submitting bats for rabies testing to the Minnesota Health Department in 2003. They too found a low level of intentional handling overall, but identified 29 of 358 bat submissions where potential human exposure occurred while capturing the bat, usually with some sort of implement.

To our knowledge, no other general population surveys related to bats and ABLV have been undertaken. Markus and Blackshaw (1998) surveyed volunteers caring for bats in Australia in 1997 about their motivations for volunteering. They asked whether ABLV and/or bat paramyxovirus were felt to be a potential threat to health. Forty-one percent considered either or both of these viruses a threat to personal health, with many stressing the need for appropriate precautions. Although not directly comparable, this might indicate a lower risk perception of bats in volunteer handlers at that time compared to participants in our survey, where 96% felt that bats posed some risk to human health, with 51% indicating moderate-to-high risk.

Studies on rabies and bats have found varying levels of knowledge in different populations. Robertson et al. (2011) interviewed a convenience sample of people at high risk of interactions with bats in Thailand in 2009. They found a low level of awareness of bat-transmitted rabies and identified that more than a quarter of their participants had been bitten or scratched by a bat. Similar to our study, knowledge of rabies was not associated with potential exposure on multivariate modeling. Piyaphanee et al. (2010) surveyed a convenience sample of non-Southeast Asian backpackers in Bangkok, Thailand, about rabies in general. Fifty-three per cent of their sample identified that rabies could be transmitted by bats. Kikuti et al. (2011) surveyed school children and teachers in Brazil immediately after a 50-min lecture on rabies and its prevention and found a high level of knowledge at this time point, including awareness that bats are able to transmit rabies.

Our findings are likely to be subject to volunteer bias. Despite the statistical generalizability of our sample in terms of age and gender, it is likely that people with some interest in bats responded to the survey, given the response rate of 24% of eligible people contacted. The levels of knowledge and/or risk perception are therefore likely overestimated. However, this should not impact on the relationships between these variables and the intention to handle bats.

Some selection bias is possible because of the exclusion of participants without fixed household phones. While it is unlikely that excluding those who own a mobile phone only (as compared to our participants who owned a landline with or without a mobile phone as well) would introduce a significant amount of bias, excluding people who do not own a phone at all is likely to have selected those with higher socioeconomic status than the general population. Indeed, the proportion of participants currently employed was higher than the general population (63% vs. 53%) (Australian Bureau of Statistics 2007). Therefore, knowledge and risk perception may have been overestimated, but this is unlikely to impact on their relationship with intention to handle bats. Certainly employment and education, while demonstrating some significant relationships with the outcome variables on univariate analysis, were not associated with intention to handle on multivariate modeling and were therefore not included in the final model.

A further limitation may have been imposed by the nature of the questionnaire. The knowledge, risk perception, and intention to handle scores were likely to be dependent to some extent on the questions asked and the scenarios given. A spectrum of questions and scenarios were deliberately included, and aggregate measures were calculated to avoid placing excess emphasis on single questions or scenarios; however, the number of questions and scenarios was limited to restrict the length of the interview required to complete the questionnaire. This may have lead to some misclassification of the intended outcomes. However, thematic analysis of the open question responses did seem to validate the conclusions reached based on the risk perception and intention to handle scores.

Conclusions

Our findings that the surveyed adult population of South East Queensland has a high basic knowledge of bats and ABLV, but that level of knowledge is not related to the intention to handle bats, is important for the prevention of future potential exposures. We recommend that future public health campaigns in Australia particularly focus on strengthening the communication of risk to humans and to bats from handling by nonvaccinated, nontrained handlers, and that younger adult males be a particular target group for such messages. Suitable alternative measures to handling should be included. The intentional handling of bats by community members related to those circumstances where people are unable to wait for the assistance of a trained and vaccinated handler should be given attention in these future campaigns, while recognizing that potential exposure in these situations will not always be preventable.

This study was undertaken in an Australian population with regard to ABLV, however the results of community member surveys about bats and rabies in other countries (Liesener et al. 2006, Robertson et al. 2011) suggest our findings about the relationship between risk perception and intention to handle bats may be generalizable outside Australia.