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Abstract

  1. Top of page
  2. Abstract
  3. Patients and Methods
  4. Results
  5. Discussion
  6. Declaration of Interests
  7. References

Objective To assess the awareness of the mode of rabies transmission, travel-associated rabies risk, and adequate preventive measures among French travelers.

Methods Three hundred travelers were administered a detailed questionnaire prior to pretravel advice, addressing their knowledge, attitudes, and practices (KAP) with respect to animal-related injuries and rabies risk. Two hundred and nine were administered a post-travel questionnaire by telephone, addressing the occurrence of contacts with animals during travel.

Results Countries visited were at risk for rabies in 84.7% of the cases. Only 6.7% of travelers knew that the risk of rabies was important, while 40.1% considered it moderate or low. Dog bites appeared to be a well-known mode of transmission of rabies. By contrast, licks on broken skin or contamination of the mucous membrane with saliva (10%) and scratches (0.7%) were rarely known. Cats (23.7%), foxes (28.3%), monkeys (10.3%), and bats (5.0%) were rarely mentioned as possible rabies vectors. Only 50.7% of travelers were aware of the preventive vaccination. Approximately 57.6% of individuals traveling to rabies–endemic countries presented to the clinic less than 21 days before departing, rendering a complete preventive vaccination against rabies unfeasible. Immediate washing of the injury with water and soap was mentioned by only 3.0% of individuals and self-disinfection with antiseptics by 21.3%. Of those who traveled in a rabies-risk country, 3.8% declared that they had been attacked by animals; however, none was injured. Animal encounters were frequent with dogs (53.8%), monkeys (39.5%), bats (17.9%), and cats (15.4%).

Conclusions The KAP of French travelers with regard to travel-associated rabies risk need to be improved, particularly regarding the prevention of animal bites, postbite measures, and their urgency.

Rabies is a nearly 100% fatal disease that can be efficiently averted by preventive immunization, avoiding contact with animals and postexposure prophylaxis. According to the Rabies Reference National Center, 20 imported rabies cases were recorded in France from 1970 to 2004 and 80% of these cases resulted from animal-related injuries acquired in Africa.1,2

Studies addressing the knowledge of rabies risk in travelers are scant. Two studies were conducted in US long-term residents in rabies-endemic countries3,4 and one in 30 travelers from Ireland.5 All demonstrated a low awareness of rabies risk among travelers. Several general studies on knowledge, attitudes, and practices (KAP) in travel-related infectious diseases were conducted in different countries but only addressed the traveler’s global perception of the risk of rabies at their destination. Rabies risk perception was shown to be largely unknown.6–9 Therefore, the purpose of the current study was to assess the awareness of the modes of rabies transmission, travel-associated rabies risk, and adequate preventive measures among French travelers from Marseille. This was done using a detailed questionnaire prior to pretravel advice and again upon the travelers’ return home.

Patients and Methods

  1. Top of page
  2. Abstract
  3. Patients and Methods
  4. Results
  5. Discussion
  6. Declaration of Interests
  7. References

A prospective study was conducted in the Marseille Travel Medicine Centre (Hôpital Nord) from June 1 to October 31, 2007, among a cohort of 300 travelers seeking pretravel advice. At that visit, each participant was administered (individually) an oral questionnaire addressing the KAP of travelers with respect to animal-related injuries and rabies risk, before the medical information was given. Inclusion criteria were participants preparing to visit a foreign country and who were at least 18 years of age.

The data collected included demographics, travel characteristics, and KAP concerning animal-related injuries and rabies and preexposure rabies vaccination status. Items were chosen based on World Health Organization (WHO) guidelines,10 and questionnaires were pilot tested among travelers at the Marseille Travel Medicine Centre.

Countries posing a potential rabies risk for travelers were determined from recent published studies and from the WHO and Centers for Disease Control sources as described elsewhere.11 Travelers were administered a post-travel questionnaire by telephone after they had returned home following their stay abroad. This post-travel questionnaire addressed the occurrence of contact with animals during their travel.

Data analysis was carried out using EpiInfo 6.0 software (Centers for Diseases Control and Prevention, Atlanta, GA, USA). Differences in proportions were analyzed using a chi-square test. The Student t-test and the Kruskal–Wallis test were used to compare continuous variables. A p value ≤0.05 was considered significant.

Results

  1. Top of page
  2. Abstract
  3. Patients and Methods
  4. Results
  5. Discussion
  6. Declaration of Interests
  7. References

Demographics

The ratio of males to females in the study was 0.7. The mean age of individuals was 36.5 years, ranging from 18 to 74. Most travelers were in the age range of 18 to 39 years (62.3%). Most travelers were born in France (79.7%), were living in urban area, and had an education level equal to or higher than a baccalaureate degree (81.3%). Approximately 12.7% of the travelers were born in countries endemic for rabies, and 38.3% of individuals stated that they had a pet at home (Table 1).

Table 1.  Demographics of 300 travelers seeking pretravel advice in Marseille Travel Medicine Centre
 n (%)
  1. CAP = certificate of study; BEPC = Brevet d’Etudes.

Sex
 Male124 (41.3)
 Female176 (58.7)
Age class (y)
 18–39187 (62.3)
 40–5998 (32.7)
 ≥6015 (5.0)
Birth country
 France239 (79.7)
 Algeria9 (3.0)
 Comoros9 (3.0)
 Senegal5 (1.7)
 Ivory Coast3 (1.0)
 Others32 (11.0)
Place of current residence
 ≥5,000 inhabitants251 (83.7)
 <5,000 inhabitants49 (16.3)
Study level
 <CAP20 (6.7)
 CAP15 (5.0)
 BEPC21 (7.0)
 Baccalaureate30 (10.0)
 University214 (71.3)
Pet owner
 Yes115 (38.3)
 No183 (61.7)

Travel Characteristics

Countries visited were at risk for rabies in 84.7% of the cases. Regions visited were sub-Saharan Africa (55.6%), Asia (19.8%), Latin America and the Caribbean (13.9%), Indian Ocean Islands (7.1%), and other regions (3.6%). The top five countries were Senegal (59 travelers), Kenya (22), Mali (15), French Guyana (14), and Thailand (13). The majority of participants (52.1%) were traveling for tourism (tour operator, 25.7%; self-organized hotel, 15.7%; and backpacker, 10.7%), while the remainder traveled for business purposes/study/missionary/volunteer (26.0%) or to visit friends and relatives (20.0%). Only 16.3% of individuals traveled alone, while most participants traveled in pairs (28.7%), families (28.3%), or in a group (26.3%). The majority of travelers (258) had travel duration of less than 6 months with a mean travel duration of 22.6 days (range 6–120 d). A proportion of 16.8% traveled for 10 days or less, 50.3% traveled for 11 to 28 days, and 32.9% for 29 days and more. A subset of 39 travelers consulted before expatriation and the remaining 3 were traveling permanently for business. Only 1% of travelers were vaccinated against rabies before traveling. Of travelers who traveled to visit friends and relatives, 32.8% originated from countries endemic for rabies.

Knowledge Assessment

The vast majority of travelers claimed to possess the basic knowledge of what rabies is (83.7%) and that it is a severe disease (89.9%). When asked about the risk of rabies in their destination country, 34.7% of travelers to rabies-free countries thought that they would be exposed to a risk of rabies, and only 6.7% of travelers to rabies-risk countries knew that the risk of rabies was important, while 40.1% considered it to be moderate or low. Most travelers clearly identified bites as a mode of rabies transmission. Other modes of transmission, like licks on broken skin or contamination of mucous membrane with saliva and scratches, were rarely reported on the questionnaire, and 11.0% of travelers had no idea about how rabies could be acquired (Figure 1). Dogs were well known as a vector of rabies (88.3%). However, cats and foxes were mentioned as possible rabies vector by only 23.7% and 28.3% of individuals, respectively. Only 10.3% of travelers mentioned monkeys as a possible vector and 5.0% mentioned bats (Figure 2). When asked how to avoid rabies risk, only 50.7% of travelers mentioned preventive vaccination and only 42.3% mentioned by avoiding animal contact. One in every four travelers declared that he did not know how to prevent rabies (Table 2).

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Figure 1. Possible modes of rabies transmission, as described by 300 travelers seeking pretravel advice in Marseille Travel Medicine Centre.

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Figure 2. Possible rabid sources, as described by 300 travelers seeking pretravel advice in Marseille Travel Medicine Centre.

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Table 2.  Knowledge assessment of 300 travelers seeking pretravel advice in Marseille Travel Medicine Centre, with respect to animal-related injuries and rabies risk
 n (%)
Do you consider having a basic knowledge about what  is rabies?
 Yes251 (83.7)
 No49 (16.3)
How severe is rabies?
 Severe disease267 (89.9)
 Mild disease7 (2.4)
 No idea23 (7.7)
How do you evaluate the risk for rabies in your destination  country?
 Travelers to rabies-free country46
  No idea14 (30.4)
  No risk16 (34.8)
  Low risk10 (21.7)
  Mild risk6 (13.0)
  High risk0
 Travelers to rabies-endemic countries254
  No idea97 (38.2)
  No risk38 (15.0)
  Low risk61 (24.0)
  Mild risk41 (16.1)
  High risk17 (6.7)
Do you know how to avoid rabies?
 Preexposure vaccination152 (50.7)
 Avoiding animal contact127 (42.3)
 Drugs3 (1.0)
 Animal’s vaccination5 (1.7)
 No idea74 (24.7)

Acceptability of Preventive Vaccination Against Rabies

When asked if they would accept a preventive vaccination against rabies if proposed by the medical advisor before their trip, 42.8% of travelers answered “yes.” Reasons for refusal of preventive vaccination were mainly low benefit/risk for rabies (55.0%), high cost (25.7%), and adverse vaccine reaction (8.2%). In individuals traveling to rabies-risk countries, the median time between travel clinic visit and planned date of travel departure was 29 days (range 4–116 d) in expatriates and 19 days (range 2–112 d) in other travelers. Thirty-six percent of individuals traveling to rabies-endemic countries for expatriation presented to the clinic less than 21 days before departing, while the number was significantly higher (57.6%) for other travelers (p = 0.02).

Attitude Regarding a Possible Animal-Related Injury During Travel

Immediate washing of the injury with water and soap was only mentioned by 3.0% of individuals and self-disinfection with antiseptics by 21.3%. Fortunately, 86.3% declared that they would immediately consult a doctor in the country of acquisition. However, 5.3% answered that they would make a call to France to seek advice. An even smaller group (2.3%) stated that they would stop their trip and return to France to seek care. The majority of travelers said that they would accept injection of rabies immunoglobulin (RIG) if proposed by the local medical staff (90.5%). However, 6.1% considered RIG dangerous and 1.4% considered it unnecessary.

Post-Travel Questionnaire

Of the 300 travelers included in the present study, 219 (73%) were contacted by telephone upon returning home. Of these, 10 individuals renounced travel. Only 209 participants actually traveled. The remaining travelers were expatriates (15%), had a planned date of return after the conclusion of the study period (4.3%), or were lost to follow-up. None of the 209 travelers were injured by an animal during their trip. Of those who traveled in a rabies-risk country, four were vaccinated against rabies (1.9%) and seven (3.8%) declared to have been attacked by an animal, but none was injured. All attacked travelers originated from a nonendemic rabies country. The numbers were too small to carry out any statistical analysis according to the travel destination. When asked about animal encounters while traveling in rabies-risk countries, 105 mentioned dogs (53.8%), 77 mentioned monkeys (39.5%), 35 mentioned bats (17.9%), and 30 mentioned cats (15.4%).

Influence of Demographics and Travel Characteristics on the KAP of Travelers With Respect to Animal-Related Injuries and Rabies Risk

The mean overall knowledge score with respect to animal-related injury risks and rabies among travelers was 42.8% (SD 12.1). The mean overall score was significantly higher in males and individuals with a university degree. Travel for the purpose of visiting friends and relatives was significantly associated with a lower mean overall knowledge compared to other reasons for travel. Whether or not the country of origin and country of destination were endemic for rabies had no significant influence on the overall knowledge scores (Table 3).

Table 3.  Mean overall knowledge score with respect to animal-related injuries and rabies risk as well as the characteristics of 300 travelers seeking pretravel advice in Marseille Travel Medicine Centre
 Score, % correctp
Sex
 Male44.90.013
 Female41.4 
Age class (y)
 18–3943.3 
 40–5942.70.171
 ≥6037.3 
Birth country
 Endemic for rabies43.10.891
 Nonendemic for rabies42.8 
Place of current residence
 5,000 inhabitants43.40.710
 <5,000 inhabitants42.7 
Study level
 Baccalaureate or less37.60.001
 University44.9 
Pet owner
 Yes44.30.094
 No41.9 
Travel destination country
 Endemic for rabies43.20.855
 Nonendemic for rabies40.5 
Reason for travel
 Tourism (tour operator)40.6 
 Tourism (self-organized hotel/backpacker)45.20.001
 Business/study/missionary/volunteer47.0 
 Visiting friends and relatives37.3 
Group size
 Alone42.5 
 Couple44.30.540
 Family40.5 
 Group43.6 
Travel duration (d)
 <1042.6 
 11–2842.10.891
 >2942.1 
 Expatriation45.3 

Discussion

  1. Top of page
  2. Abstract
  3. Patients and Methods
  4. Results
  5. Discussion
  6. Declaration of Interests
  7. References

Demographic and travel characteristic of individuals in our study did not widely differ from those of the larger general KAP study on travel-related infectious diseases involving 5,067 Europeans travelers, suggesting that our sample is representative of the west European travelers in terms of age, gender, reason for travel, and duration of travel.6 However, our study was based on a population of travelers identified from a single travel clinic in Marseille. This may well have resulted in some significant biases in participant selection as evidenced by a higher proportion of travelers to Sub-Saharan Africa in our cohort, probably due to the requirement for such destinations of yellow fever vaccination, which is available in France from travel international vaccination centers only. Our results therefore cannot be extrapolated to all French travelers but provide valuable information for travel medicine specialists seeing such travelers at their travel clinic.

Animal-associated injuries in travelers occurring in rabies-endemic countries are not an infrequent event11,12 and pose a serious health threat to individuals visiting such areas.13 In the present study, a great lack of knowledge regarding rabies risk in the visited countries was observed, which is consistent with previous studies.3–9 As expected, dog bites appeared to be well known as a mode of transmission of rabies. In contrast, licks on broken skin, contamination of mucous membranes with saliva, and scratches were rarely known. In addition, cats, foxes, monkeys, and bats were rarely mentioned as possible rabies vectors. Interestingly, in a previous work, monkeys were identified as a significant source of injury among travelers, especially in Asia.11 It is therefore necessary to increase the knowledge of travelers on the presence of rabies in the country they are planning to visit and of modes of transmission distinct from the classical dog bite injury.

Immediate washing of the injury with water and soap and self-disinfection with antiseptics were not known by most travelers in this study. Travelers should be informed of these simple measures that they should apply before consulting a doctor in the country of acquisition.

Preventive vaccination against rabies is classically proposed to long-term travelers and tourists who are planning to stay in rural rabies–endemic areas.14 However, it was recently shown in a GeoSentinel network-based study11 that animal-associated injuries occurring in rabies-endemic countries were not necessarily associated with long-term travel. In fact, 50% of travelers had a travel duration of less than 1 month, while 85% had traveled for less than 3 months. In addition, when the reason for travel was examined in all cases reported to GeoSentinel, it was determined that traveling for tourism was associated with an increased likelihood of being injured by an animal. This would suggest that the usual type of trip that most travelers are likely to undertake would pose a risk for animal-related injuries and potentially for rabies. In the present study, it was observed that only 42% of travelers would accept a preventive vaccination against rabies if proposed by the medical advisor prior to their trip. WHO recommends a preexposure vaccine schedule consisting of one dose of intramuscular full dose or 0.1 mL of intradermal dose injected on days 0, 7, 21, or 28.10 More than 57% of travelers to rabies-endemic areas presented to the clinic less than 3 weeks before departing, rendering a complete preventive vaccination against rabies unfeasible, which is consistent with the general KAP study in European travelers.6 Completing the series at the destination appears very unlikely in short-term travelers. This correlates with a recent retrospective study in which a very low rate of rabies preexposure vaccination coverage was observed in returned travelers who experienced animal-related injuries in countries endemic for rabies.15 Although preventive vaccination against rabies should be proposed to travelers to rabies-risk countries, especially when human or equine rabies immune globulins are unavailable, its weak acceptability, the 21-d vaccination schedule, and the price of vaccine makes routine vaccination unrealistic. However, intradermal rabies vaccination, which is recommended by WHO in travelers as an alternative to intramuscular vaccination,16 was showed to be effective when administered by vaccinators with relevant experience17,18 and more readily accepted than the more expensive intramuscular schedule.19 Abbreviated intradermal schedules have been recently described in an interesting preliminary study, but additional investigation with a larger numbers of travelers is needed.20

Data regarding the incidence of animal-related injuries in short-term travelers are scant. In a study conducted in adult international travelers leaving Bangkok International Airport and who had spent an average of 17 days in Thailand, it was shown that 1.3% experienced dog bites, while 8.9% were licked by a dog during their stay.12 In addition, the rate of exposure to animal-associated injuries was shown to be 1.9 per 1,000 persons per year for tourists in Nepal21 and 1.6% in Israeli travelers.22 In the current study, travelers were well aware of animal-related injuries and rabies risk following the questionnaire, which improved their knowledge given that comprehensive information was provided during the pretravel encounter, and none of them experienced an injurious contact with an animal during their trip though 3.8% declared that they had been attacked by animals and a majority mentioned animal encounters. Although no conclusion could be made from our small sample, it is very likely that when adequately counseled, travelers could easily avoid animal-related injuries when visiting rabies-infected countries, rendering the problems posed by preventive vaccination and rabies postexposure prophylaxis obsolete. In all instances, the necessity to inform travelers about rabies risk means that travelers should consult a medical advisor before traveling. In a previous work, it was observed that 45% of animal-related injuries in travelers returning to Marseille occurred in North Africa.10 In the present study, there were no participants traveling to North Africa. Generally, only a few travelers to North Africa seek pretravel advice in our clinic, which is not surprising as no specific vaccination and no malaria prophylaxis are required to travel to North Africa. Information about rabies risk when traveling to North Africa could be alternatively given by general practitioners and travel agencies in Marseille.

Declaration of Interests

  1. Top of page
  2. Abstract
  3. Patients and Methods
  4. Results
  5. Discussion
  6. Declaration of Interests
  7. References

The authors state that they have no conflicts of interest.

References

  1. Top of page
  2. Abstract
  3. Patients and Methods
  4. Results
  5. Discussion
  6. Declaration of Interests
  7. References