Conceived and designed the experiments: KR BL RF SB LFP HCB SAM CER. Performed the experiments: KR BL BP SB SH. Analyzed the data: KR. Contributed reagents/materials/analysis tools: KR. Wrote the paper: KR BL RF BP SH LFP HCB SAM. Served as an interpreter and interviewer, and facilitated recruitment: BL. Facilitated collaboration with contacts in Thailand so logistics were in place for study: RF. Interviewed subjects: SB SH. Assisted with logistics: LFP HCB SAM.
The authors have declared that no competing interests exist.
Rabies is a fatal encephalitis caused by lyssaviruses. Evidence of lyssavirus circulation has recently emerged in Southeast Asian bats. A cross-sectional study was conducted in Thailand to assess rabies-related knowledge and practices among persons regularly exposed to bats and bat habitats. The objectives were to identify deficiencies in rabies awareness, describe the occurrence of bat exposures, and explore factors associated with transdermal bat exposures.
A survey was administered to a convenience sample of adult guano miners, bat hunters, game wardens, and residents/personnel at Buddhist temples where mass bat roosting occurs. The questionnaire elicited information on demographics, experience with bat exposures, and rabies knowledge. Participants were also asked to describe actions they would take in response to a bat bite as well as actions for a bite from a potentially rabid animal. Bivariate analysis was used to compare responses between groups and multivariable logistic regression was used to explore factors independently associated with being bitten or scratched by a bat.
Of 106 people interviewed, 11 (10%) identified bats as a potential source of rabies. A history of a bat bite or scratch was reported by 29 (27%), and 38 (36%) stated either that they would do nothing or that they did not know what they would do in response to a bat bite. Guano miners were less likely than other groups to indicate animal bites as a mechanism of rabies transmission (68% vs. 90%, p = 0.03) and were less likely to say they would respond appropriately to a bat bite or scratch (61% vs. 27%, p = 0.003). Guano mining, bat hunting, and being in a bat cave or roost area more than 5 times a year were associated with history of a bat bite or scratch.
These findings indicate the need for educational outreach to raise awareness of bat rabies, promote exposure prevention, and ensure appropriate health-seeking behaviors for bat-inflicted wounds, particularly among at-risk groups in Thailand.
Rabies is a fatal encephalitis caused by lyssaviruses. Evidence of lyssavirus circulation has recently emerged in Southeast Asian bats. We surveyed persons regularly exposed to bats and bat habitats in Thailand to assess rabies‐related knowledge and practices. Targeted groups included guano miners, bat hunters, game wardens, and residents/personnel at Buddhist temples where mass bat roosting occurs. Of the 106 people interviewed, 11 (10%) identified bats as a source of rabies. History of a bat bite/scratch was reported by 29 (27%), and 38 (36%) expressed either that they would do nothing or that they did not know what they would do in response to a bat bite. Guano miners were less likely than other groups to indicate animal bites as a mechanism of transmission (68% vs. 90%, p=0.03) and were less likely to say they would respond appropriately to a bat bite or scratch (61% vs. 27%, p=0.003). These findings indicate a need for educational outreach in Thailand to raise awareness of bat rabies, promote exposure prevention, and ensure health‐seeking behaviors for bat‐inflicted wounds, particularly among at‐risk groups.
Rabies is an exceptionally fatal encephalitis caused by Rhabdoviruses in the Lyssavirus genus. Transmission typically occurs when broken skin is contaminated with saliva from an infected mammal—usually in association with a bite but in rare instances by scratches. The most well-known and ubiquitous lyssavirus is the rabies virus (RABV), which circulates in New World bats and both Old and New World terrestrial mammals. The vast majority of human rabies cases worldwide are transmitted by dogs infected with RABV. A lesser known member of the genus is the Mokola virus, which has been isolated from a number of terrestrial mammals in Africa (most notably shrews) and has caused at least two human cases
Rabies is a major public health problem in Asia. Of the estimated 55,000 human cases that occur annually worldwide, more than half occur in Asian countries
Historically in Southeast (SE) Asia, animal-based prevention efforts for rabies have almost exclusively been centered on dogs. Most reported human cases in the region are traced to these animals either through an exposure history or through molecular or antigenic subtyping of variants from rabid human patients
Within the last ten years, however, interest in bats and their role in lyssavirus transmission has increased in the region. The discovery of the Australian Bat Lyssavirus (ABLV) in Australian flying fox bats (
Routine surveillance for bat rabies is lacking in Asia and as a consequence, understanding is limited regarding the extent of lyssavirus circulation among SE Asian bats and the impact on animal and public health. However, evidence thus far raises pressing questions about human health risks. The potential implications of bat rabies are particularly salient in SE Asia because human-bat interaction occurs routinely in many locales. Bat guano is regularly mined from caves for use as a fertilizer. Hunting of bats for sale and personal consumption occurs as well, despite laws to stop this practice. The presence of large numbers of bats at many Buddhist temples also promotes exposures, as these sites are focal points for commerce, tourism, and religious expression.
Because the severity of skin trauma inflicted by bats is usually minor and unlikely to prompt a medical visit on the basis of physical injury alone, public knowledge of appropriate health-seeking behaviors following a bat exposure is especially important in preventing cases of bat-borne rabies. Rabies postexposure prophylaxis (PEP) for bat bites and scratches, as recommended by both the World Health Organization (WHO) and the U.S. Advisory Committee on Immunization Practices (ACIP), includes thorough wound washing and the administration of rabies immune globulin (in non-immunized individuals) and rabies vaccine administered in a series of doses
Little is known about the extent of bat-specific rabies awareness in SE Asia. To assess the knowledge and practices of individuals who are most at-risk of bat exposures in Thailand, we surveyed persons who regularly come in contact with bats or bat dwellings through occupational activities and other practices. We sought to elucidate gaps in knowledge that potentially have bearing on rabies prevention, describe the occurrence of bat-associated exposures in this population, and explore factors associated with bat exposures that are of potential consequence to lyssavirus transmission.
The desired sample size was 200 individuals. Surveyed individuals were a convenience sample of adults who collect guano from caves, engage in bat hunting, work or reside at temples that serve as sites for mass bat roosting, or work as game wardens responsible for monitoring and protecting bat caves. Engagement in at least one of these activities within the last 5 years and being 18 years or older were inclusion criteria for participation. Individuals were recruited from eight provinces as shown by
The study design and consent process was approved by the Institutional Review Board (IRB) at CDC (protocol# 5709). All participants were verbally informed of the study's purpose and assured that their responses would be kept anonymous, even if they engaged in illegal activities. Oral consent was obtained to ensure anonymity and accommodate illiterate participants, and was documented by the interviewer electronically via personal digital assistants (PDA) prior to administering the survey. This method of obtaining informed consent was approved by CDC's IRB.
A 41-item structured questionnaire was developed in English and translated and reviewed by native Thai speakers employed by the office of the U.S. CDC, International Emerging Infections Program in Bangkok. The questionnaire was designed to be administered in Thai via face-to-face interviews, with responses entered in PDAs using GeoAge FAST software. Not all questions provided data used in this study. The questionnaire was developed based on socio-ecological reasoning about gaps in rabies knowledge that potentially translate into failed prevention on the individual level.
Data were collected on demographics; primary bat-associated activity and years of experience; history of rabies vaccination; and type and frequency of bat exposures such as cave entry, direct contact with bats, bites and scratches from bats, and bat consumption. Individuals who reported receiving rabies vaccination were asked to indicate whether it was in direct response to an animal exposure (i.e. PEP) or for pre-exposure immunization (PreP), which is a vaccination series most often administered to people who have a relatively high likelihood of rabies virus exposure due to occupational risks or other factors. Those who reported receiving PreP were asked to describe its administration and only those who indicated receiving a series of injections spaced over multiple days were counted as having PreP.
To assess rabies-related knowledge, participants were asked to rate their understanding of the disease as either “little or none”, “basic”, or “extensive”; explain how humans acquire the disease, and identify animal sources of the disease. Each knowledge question was evaluated independently, and the validity of a participant's self-reported knowledge level was not verified using other responses. Participants were also asked to describe the severity of rabies. Only responses that emphasized death or profound suffering with no suggestion that recovery was likely were considered evidence that the participant recognized rabies as being severe. Awareness of other diseases that humans can get from bats was also elicited.
To assess health-seeking practices following transdermal bat exposures, participants were asked about actions they would take if they were bitten or scratched by a bat. Responses to this open-ended question were compared to a similar question later asked about actions a person should take following a bite from a potentially rabid animal, based on the participant's own understanding of what constitutes a potentially rabid animal. Questions that were specifically asked about bats preceded all questions asked about rabies to minimize reporting bias, and whenever feasible, participants were asked open-ended questions to minimize the interviewer's influence on responses. Participants were also interviewed away from other people. Interviewers were instructed to not ask questions in a leading manner and to allow as much time as necessary for participants to answer.
Survey responses were transferred to a computer, exported into Microsoft Excel, and then imported into SAS version 9.2 for analysis. Data were summarized using descriptive statistics and comparisons by bat-associated activity group were made using Chi-square or Fisher's exact test. Multivariable logistic regression analysis was used to explore factors independently associated with being bitten or scratched by a bat. Variables related to the outcome at p-values≤0.25 were included in the model. Crude and adjusted odds ratios (OR) with 95% confidence intervals (CI) were calculated. Associations were statistically significant at p-values less than 0.05.
The study was conducted during August 3–18, 2009. A total of 106 people were interviewed. Interviews lasted an average of about 10 minutes. Demographic characteristics, history of rabies vaccination, and primary bat-associated activity of the participants are described in
Category | Subcategory | Value |
No. (%) male | – | 86 (81) |
Age in years, median (range) | – | 44 (20–75) |
No. (%) with < primary level |
– | 68 (64) |
No. (%) with >15 years of experience |
– | 41 (40) |
Bat-associated activity, No. (%) | Temple work/residence | 41 (39) |
Guano mining | 28 (26) | |
Game warden | 19 (18) | |
Bat hunting | 18 (17) | |
Prior rabies vaccination, No. (%) | None | 73 (69) |
PreP |
8 (8) | |
PEP |
25 (24) |
Percentages are rounded.
Six years or less of formal education.
More than 15 years of experience in bat-associated activity.
PreP = Pre-exposure prophylaxis.
PEP = Post-exposure prophylaxis.
Thirty-one percent of participants reported a history of receiving either rabies PreP (7.5%) or PEP (23.5%) within their lifetimes. Of those who had received rabies PEP, 96% reported that they had been vaccinated in response to a dog exposure and 4% for a cat exposure. No participants reported receiving PEP for a bat exposure and none reported receiving both PreP and PEP. There were no statistically significant differences between activity groups with respect to rabies vaccination.
Rabies-related knowledge response | Temple workers/residents (n = 41) | Guano miners(n = 28) | Game wardens(n = 19) | Bat hunters (n = 18) | Total(n = 106) |
Reported having little or no rabies knowledge | 39 | 77 | 53 | 65 | 54 |
Indicated animal bites as mechanism of transmission | 95 | 69 | 89 | 94 | 85 |
Described rabies as severe | 83 | 65 | 89 | 71 | 78 |
Identified bats as a rabies source | 5 | 7 | 16 | 22 | 10 |
Advocated action | For a bat exposure | For exposure to a potentially rabid animal | p-value |
Seek medical care/rabies PEP | 26 | 95 | <0.0001 |
Wash wound |
43 | 33 | 0.09 |
Nothing/don't know | 36 | 2 | <0.0001 |
Traditional care |
0 | 3 | 0.24 |
Other |
8 | 1 | 0.04 |
Comparing the proportion of participants who advocated a given action for a bat exposure with the proportion who advocated the same action for an exposure to a potential rabid animal.
Includes cleaning the wound with water, soap, and/or a common antiseptic agent (e.g. betadine).
Includes prayer or visiting a traditional healer.
Includes bleeding the wound, bandaging, or using topical home remedies (e.g. local herbs).
Exposure Type | No.(%) ever having exposure | No.(%) having exposure >5×/year |
Inside bat cave or roost area | 96 (91) | 61 (58) |
Direct bat contact | 63 (69) | 29 (27) |
Bat consumption | 57 (54) | 11 (10) |
Bat scratch | 23 (22) | 6 (6) |
Bat bite | 18 (17) | 2 (2) |
Category | Subcategory | N(%) | OR |
aOR |
Bat-associated activity | Temple worker/resident | 7 (17) | ref | ref |
Guano miner | 11 (39) | 3.1 (1.0–9.6) | 6.7(1.8–25.6) | |
Game warden | 5 (26) | 1.7 (0.5–6.4) | 3.7 (0.8–16.8) | |
Bat hunter | 6 (35) | 2.4 (0.7–8.7) | 12.0 (2.0–72.0) | |
Self-assessed rabies knowledge | Little or none | 21 (38) | 3.2 (1.2–8.0) | 2.7 (1.0–7.5) |
Basic and above | 5 (26) | ref | ref | |
Frequency of being in a cave/roost area | ≤5×/year | 7 (16) | ref | ref |
>5×/year | 22 (36) | 3.1 (1.2–8.0) | 10.6 (2.9–39.7) |
OR (95% CI) = Odds Ratio (95% Confidence Interval).
aOR = Adjusted Odds Ratio.
In this survey among persons at risk for bat exposure in Thailand, we found that although general awareness of rabies transmission and severity were relatively high, awareness of bat rabies in particular was low, with only 10% of participants identifying bats as a potential source of rabies and 36% failing to say they would take any specific action if bitten or scratched by a bat. Bat exposures conducive to potential lyssavirus transmission were also common in this population and were reported by members of all four activity groups, supporting more than just a theoretical risk for these types of incidents. We found that guano miners reported the highest frequency of transdermal bat exposures, were the least knowledgeable about rabies, and were the least likely to say they would respond to bat exposures in a manner that would ensure rabies prevention. Based on these findings we conclude that of the groups we surveyed, bat rabies has the greatest potential impact on guano miners. The potential risk associated with guano mining is even more stark given that moribund bats (i.e., those most likely to be rabid) normally fall to the floor of caves, where they can readily come in contact with someone collecting bat droppings by hand. The effectiveness of any bat-borne rabies prevention strategy may hinge upon how well it diffuses into communities where guano mining regularly occurs.
Education at the community level is an important strategy in the prevention of human rabies
To date, there have been no reported cases of human rabies cases associated with bats in Thailand. One plausible explanation is that the prevalence of bat lyssaviruses in SE Asia is so low that humans are rarely if ever exposed to these pathogens. It is also possible that the prevailing assumption about dogs as the usual source of rabies leads patients and their family members to overlook relevant bat encounters when recounting animal exposures, resulting in misdiagnosis or misattribution. Additionally, the rate of human rabies vaccination in the population may be high enough to protect many people against bat rabies. In our study, we found that almost a third of all participants reported a history of rabies vaccination, mostly as a result of dog-associated PEP. This suggests that the percentage of individuals in our study population with at least some lyssavirus immunity is relatively high and may help account for why bats have yet to be linked to any human rabies cases in the country. However, immunity levels could change if PEP use becomes more conservative in the future. Currently, funds annually spent on the purchase of human rabies biologics by the Thai government are quite substantial
There are some limitations to our study that should be noted. First, it is unlikely that our relatively small convenience sample is representative of all persons engaged in bat-related activities in Thailand. Our findings may have also been subject to reporting bias, since guano miners and bat hunters may have been less willing than others to answer questions truthfully due to the illegal nature of their work. This potential bias may have led participants to understate their years of experience, which could explain why this variable was not found to be associated with a history of transdermal bat exposures. Estimated participation rates for these two groups were also much lower than the other two groups (participation rates were hard to definitively ascertain because participation was ultimately premised on self-identification). Additionally, we classified individuals based on their self-reported
Our findings have relevance to zoonotic diseases other than rabies. SE Asian bats have been linked to the encephalitis-causing Nipah virus and Hendra virus
The authors thank Dr. Robert Gibbons and the US Department of Defense's Armed Forces Research Institute of Medical Sciences (AFRIMS); Dr. Rattiya Naksuwan from the Thailand Ministry of Agriculture; Parnkaew Rattanasilpkancharn from the Thailand Ministry of Health; Dr. Sumalee Boonmar, Benchawan Pongurgsorn, Pongpun Sawatwong, and Manoon Hirunsalee from CDC-Thailand IEIP; and Dr. Amy Turmelle, Felix Jackson, and Dustyn Palmer, of the Poxvirus and Rabies Branch, CDC.