Rabies, a viral zoonosis, is usually transmitted to humans by bites of infected animals and causes an almost uniformly fatal infection. Estimates indicate that every year more than 50,000 people worldwide die from this disease. The overwhelming majority of human rabies infections occur in tropical and subtropical areas where the virus circulates among domestic and stray animals.1,2 Countries with a high rabies endemicity include many popular tourist destinations, which annually attract about 4 million travelers from Germany alone.3 Although the factual risk of acquiring rabies while visiting these parts of the so-called developing world is low,4 as reflected for instance by the rare and anecdotal reports on cases of human rabies infections imported to Europe,5,6 travelers are prone to a substantial risk of potential exposure to the virus through animal bites or scratches.7 In a survey from Thailand, 24 of 1,882 tourists, who stayed there for an average of 17 days, were bitten by dogs and almost 9% of the visitors could recall that they experienced licks.8 In a travel clinic in Kathmandu, Nepal, during a 3-year period, 56 travelers with a possible exposure to rabies were treated, resulting in an annual incidence of 1.9 per 1,000 persons.9 Taking these figures into account, national and international guidelines recommend that the risk of rabies should be adequately addressed during pretravel health consultations,7,10 which are sought at least by most of the tourists from Europe.11,12 Appropriate rabies-specific information, however, can only be provided if the physicians or pharmacists responsible keep themselves continuously up to the professional standards.11 Therefore, in the current study we tried to assess the awareness of travel-associated rabies risks and the knowledge about adequate preventive measures including pre- and postexposure prophylaxis among experienced German travel health advisors using a detailed questionnaire.
Background Every year, millions of people travel to countries where rabies is enzootic. However, the quality of rabies-specific information provided by travel health advisors and the extent of their knowledge about pre- and postexposure prophylaxis have not been examined on a large-scale basis up to now.
Methods 5,780 German physicians and pharmacists, who identified themselves as active travel health advisors, were chosen from a database. The selected providers were asked to complete an Internet-based questionnaire. The form requested both demographic information and the assessment of different concrete scenarios, each of which featured individuals seeking pretravel advice on rabies or appropriate postexposure treatment after returning from abroad.
Results Overall, 496 physicians and pharmacists completed the questionnaire. Almost all respondents indicated that they would mention the risk of rabies and appropriate preventive measures to long-term travelers and tourists planning to visit rural areas. However, only 35% to 60% of the advisors would provide this information to individuals on business trips, package tours, or travelers in urban centers as well. The assessment of the scenarios yielded 51% to 98% of adequate advice. Potentially harmful decisions included, for instance, the failure to recommend further prophylactic measures after exposure of already vaccinated people or the fact that the necessary postexposure prophylaxis was inappropriately withheld in cases where treatment had been initially delayed.
Conclusions Although the participants of this study were well aware of the travel-associated rabies risks and provided adequate information about this health hazard to most of their clients, evident flaws exist regarding the correct assessment of specific situations in pre- and postexposure rabies prophylaxis. Our findings therefore provide important cues on topics that should be more intensely covered during future postgraduate training in travel medicine and also underline the need for more practically orientated, readily available information on specific prophylactic treatment against rabies.
The questionnaire in its first part requested demographic information on the respondents. The second “rabies-specific” part was set up in a multiple-choice format. We asked the travel health advisors: “Whom of your clients do you inform about the risk of rabies and preventive measures when traveling to countries where the disease is enzootic?” In addition, they had to provide an assessment of four concrete scenarios, all of which represented “real cases” taken from our own daily practice as travel health consultants. To evaluate its feasibility, the questionnaire was sent to 10 experts in travel medicine for a pretest. Their comments and suggestions were used to improve the form further.
To constitute a suitable study population, a database containing the names and addresses of almost 140,000 physicians and pharmacists from all parts of Germany was used and those 5,780 who identified themselves as active travel health advisers were chosen. Subsequently, a letter was sent to the selected providers informing them about the scope and the aims of the study and asking them to participate in the survey by filling in the questionnaire via Internet. The user name and password necessary for login were contained in the covering letter and were no longer valid once the form was completed and submitted. The participants could access the respective Web site for 6 weeks in May and June 2005.
Two of the authors (R.S.R. and B.W.) analyzed the obtained responses based on the policies formulated in both national13,14 and international15 guidelines for travel health advice and the suggestions given by special recommendations for pre- and postexposure prophylaxis on rabies.16,17 If the answers were completely in line with these documents, they were recorded as “adequate advice,” whereas deviations leading to a potential health hazard for the travelers were regarded as “inadequate advice.” In cases were statements were rated differently by the authors, benefit was always given to the participants of the study. As factors that might exert an influence on the responses, the travel health advisor’s profession and, as far as physicians were concerned, the medical speciality were also taken into account. In addition, consideration was given to whether or not the respondent had received a postgraduate training in travel medicine, and the degree of his or her specific experience was measured by both the number of years of activity in the field and the approximate number of travel health consultations actually provided per year. Proportions were compared by χ2 tests, and differences were regarded to be significant at the 5% level. For data analysis, the Statistical Package for Social Sciences, version 11 (SPSS Inc., Chicago, IL, USA), was applied.
Respondents’ characteristics and sources of information used for providing travel health advice
A total of 496 out of the selected 5,780 travel health advisors completed the questionnaire via Internet, corresponding to an overall response rate of 9%. The median time required to fill the form was 11 minutes, and the Web site was accessed by almost 60% of all respondents between noon and 3:00 PM or 7.00 to 10.00 PM. About 85% of those who completed the questionnaire were physicians, and 15% pharmacists. Of the physicians, almost two thirds were working in private practices, and 4%, 7%, and 6% were based in hospitals, occupational medicine agencies, and public health offices, respectively. Almost 42% of the physicians and 33% of the pharmacists had received some kind of formal, structured postgraduate training in travel medicine (Table 1). The participants of our study had been active in the field between 7 (pharmacists) and 15 (physicians in public health offices) years, and the number of travelers counseled by them annually ranged from 20 (pharmacists) to 127.5 (physicians in public health offices). Concerning the sources of information that formed the basis for providing travel health advice, the spectrum was clearly dominated by two national guidelines, namely the recommendations of the German Advisory Committee on Immunisations13 and the recommendations for vaccinations for travelers issued by the German Society of Tropical Medicine and International Health.14 Both documents were regularly used by 88 and 80% of the respondents, respectively, and 13% of them said that they usually consult both guidelines in parallel. The WHO recommendations15 were utilized by 69% of the participants. Besides these three main sources, a variety of other informational materials on travel medicine was also given consideration. Neither the respondents’ profession nor their medical speciality exerted a significant influence on usage of the information sources.
|Expertise in travel medicine||General practitioners (N = 213)||Internists (N = 73)||Occupational physicians (N = 34)||Physicians in public health offices (N = 28)||Other physicians (N = 70)||Pharmacists (N = 72)|
|Postgraduate training in travel medicine, N (%)||78 (36)||31 (42)||24 (71)||16 (57)||29 (41)||24 (33)|
|Years of experience in travel medicine (median)||12||10||11.5||15||12||7|
|Travel health consultations/year (median)||32.5||40||87.5||127.5||50||20|
Awareness of travel-associated rabies risks and knowledge about preventive measures
Figure 1 summarizes the participants’ answers to the question “Whom of your clients do you inform about the risk of rabies and preventive measures when traveling to countries where the disease is enzootic?” All respondents selected at least one out of the five categories precoded in the multiple-choice list of the questionnaire and the vast majority indicated that they are providing such information for both long-term travelers and tourists who are planning to stay in rural areas. However, only 60, 40, and 35% of all respondents would mention the rabies risk during consultations of individuals who want to visit urban centers, who had booked a package tour, or who will go to countries with high rabies endemicity on business trips. The choice of the three latter categories was significantly dependent on whether or not the respondent had received a postgraduate training in travel medicine and was also notably influenced by the number of travel health consultations provided per year.
Table 2 gives an overview on the assessment of the different travel scenarios. The first setting assumed a 22-year-old man who wants to leave for Vietnam for a 3-week vacation in 2 months. Only 2% of the participants saw no reason to address the potential travel-associated rabies risk and would, therefore, have provided inadequate advice. About 7% of the responses belonged to the category “I would tell him how he can efficiently reduce the risk of being exposed to rabies,” and 18% of the travel health advisors would include into their recommendations for rabies prevention the warning that a doctor should be consulted in the case of an animal bite. The answer “I would recommend a vaccination against rabies” was chosen by 45% of the participants, and 28% said that they would advise the man to undergo pretravel immunization against rabies if he is planning a hiking tour. The judgments of physicians did not differ significantly from those of pharmacists, but advisors with a postgraduate training in travel medicine, general practitioners, and medical doctors in public health offices tend to recommend a vaccination against rabies in this scenario more often than others.
|Scenario||Adequate advice (%)||Inadequate advice (%)||Examples for inadequacies|
|Traveling to Vietnam—recommendations for prevention of rabies?||98||2||Failure to mention rabies risk|
|Traveling to Latin America—measures after exposure of an individual previously vaccinated against rabies?||51||49||Failure to recommend further prophylactic measures after exposure; administration of RIG|
|Returned from Turkey—management of a dog bite (2 weeks ago)?||60||40*||Failure to start RPEP; RPEP started, but no RIG administered|
|Returned from India—continuation of a RPEP scheme started abroad (20 days ago)?||92||8||Failure to continue RPEP; administration of RIG without starting whole RPEP again from the beginning|
The second casuistry envisioned a young lady who is planning to work for 6 months in a development aid project in Latin America. She received three doses of rabies vaccine 1 year ago and is now asking her travel health advisor what she should do if she is exposed to the virus during her stay. Almost 49% of the answers were inadequate. The lady would have been told that she should receive rabies immunoglobulin after exposure or should not worry at all because she is definitely protected from the infection due to the preceding vaccinations. Many respondents were also under the impression that the determination of a protective titer of rabies-specific antibodies before departure would obviate the need of any postexposure prophylaxis. About 51% of the participants provided adequate advice and advocated for consultation of a physician and “booster” vaccinations against rabies if an exposure to the virus should occur. This latter possibility was particularly favored by physicians in general and travel health advisors who are actually providing more than 100 consultations annually.
In the third travel scenario, the participants were asked to imagine a man who was on vacation in Turkey and who was bitten there 2 weeks ago by a dog in his upper thigh. He received local wound treatment and a vaccination against tetanus immediately and now, after his return to Germany, wants to find out whether the measures already taken abroad were sufficient. A total of 30 individuals (6%) did not provide any answer to this casuistry, and the remaining 167 inadequate decisions comprised the following: (1) a postexposure prophylaxis against rabies is useless because dogs do not transmit this disease in Turkey (2%), (2) further measures are not warranted given that there are no signs of wound infection (6%), (3) initiation of a postexposure prophylaxis will not be effective anymore because the man was already bitten by the dog 2 weeks ago (11%), and (4) a postexposure prophylaxis should be started, but only vaccine and no rabies immunoglobulin should be administered (15%). About 60% of the respondents chose the correct answer: “I would begin a postexposure prophylaxis consisting of five vaccinations and the simultaneous application of rabies immunoglobulin once together with the first dose of vaccine.” Postgraduate training in travel medicine and the amount of experience in the field did not affect the pattern of answers and pharmacists unanimously stated that they would refer the man to a physician for further consultation.
The final setting was focused on a lady who, during a stay in India, experienced multiple bites from a cat and received vaccinations with Verorab® on days 0, 3, 7, and 14. Upon return to Germany, she consulted her local travel health advisor on the 20th day after exposure and asked what should be done now. In this case, 8% of the participants opted for inadequate solutions because they thought that rabies immunoglobulin should be applied (1%) or that the postexposure scheme had been already finished correctly in India (7%). A total of 32 physicians (7%) would start the whole postexposure treatment again from the very beginning because they were afraid of product falsification and thought the vaccine could have been stored under inappropriate conditions. A total of 299 individuals (60%) said they were not sure about the type of vaccine and would therefore try to seek further information preferably from the manufacturer before making a decision and the remaining quarter of the respondents would have given the missing fifth dose of vaccine immediately. Interestingly, this last answer, which was the most adequate one, was chosen by 53% of those advisors actually providing more than 500 travel health consultations per year.
Up to now, the information available on travel health advisors’ awareness of rabies risks and appropriate preventive measures is scanty and to our knowledge only one publication exists that addresses these issues in greater detail by questioning general practitioners.11 Therefore, we conducted the survey described here and decided not to restrict our investigation to members of a certain medical speciality but to include physicians from a variety of disciplines as well as pharmacists, who represent an important primary source of travel health information in Germany and other European countries.18 The interpretation of the data obtained has to take into account several important general factors. First, the study population was chosen from a database containing the names and addresses of almost 40% of all German physicians and pharmacists, and the selection process was based on a previous self-identification as active travel health advisor. Second, the overall response rate of 9% might be partly attributable to the fact that the selected providers were simply sent a letter informing them about the scope and the aims of the survey without any prior consultations ensuring their participation. Furthermore, no reminders were used and the form had to be completed within 6 weeks. Third, the investigation was Internet-based, making online access a prerequisite. In this respect, one should bear in mind that in 2003 already 79% of German general practitioners and internists reported that they have personal online access19 and that this rate has increased to 100% in a more recent study (K. Dehmel, T. Hummel, Marburg, Germany, 2005 Sept., personal communication). A further point worth mentioning is the objection that filling in a questionnaire does not reflect the knowledge readily available to the respondent.11,18,20 Finally, the participants in our survey had been active in the field of travel medicine for many years and currently counseled a median number of 40 travelers annually. Thus, they constitute a cohort with a profound expertise in travel medicine, and the level of rabies-specific knowledge is probably considerably lower in other less experienced groups that also provide travel health advice in Germany.
Given this general background, the physicians and pharmacists who responded to our questionnaire were well aware of the fact that exposure to rabies presents a substantial health hazard to travelers visiting countries where the disease is enzootic. On the one hand, only 2% of the advisors did not fulfill the minimal requirements of national and international recommendations13–15 for providing pretravel health advice because they said they would not mention preventive measures against rabies in the course of a consultation with a traveler planning to visit Vietnam. This rate is by far more favorable than figures reported by other groups previously.11,21,22 On the other hand, the participants of our study also indicated that they do not inform all categories of travelers equally about the risk of rabies in countries where the disease is enzootic. In contrast to the relevant guidelines,13–15 they fail to mention the possibility of exposure and the need of preventive measures in 40% to 65% of all consultations sought by travelers to urban centers, on package tours, or business trips, thereby neglecting that dog bites, scratches, and licks mostly occur in cities rather than in rural areas8 and that at least one of the most recent cases of human rabies infection imported to Europe was acquired on a business trip to India.23
The respondents to our questionnaire were generally very open minded about the use of preexposure vaccination against rabies. About 28% of them would advise a man who is planning a hiking tour in Vietnam to undergo such a treatment. This rate is similar to the results of a previous British survey on the appropriateness of medical advice for trekkers. Here, among individuals who wanted to visit Nepal, 27% were told that a vaccination against rabies should be considered. However, the British colleagues only provided this advice to 1 of 45 travelers leaving for Morocco and to none of those heading for India.12 Whereas all decisive authorities agree on the need of preexposure rabies prophylaxis in certain groups of travelers (eg, hikers and all those who will stay for a long time or will not have immediate access to appropriate medical care), serious doubts exist about the usefulness of a routine preexposure vaccination. None of the relevant guidelines13–15 currently advocate for this preventive measure in general, taking rather unfavorable cost–benefit analyses24 and a series of other considerations into account. Thus, it is one of the notable findings of our investigation that almost half of the participants would nevertheless recommend a general preexposure vaccination to their clients before leaving for countries like Vietnam. In this respect, the respondents perhaps adopted the view of a recent influential German consensus paper on rabies vaccination in travelers, which favored a more widespread use of preexposure immunization.25
As far as we know, the expertise of travel health advisors on postexposure prophylaxis against rabies had not been previously investigated in detail. The assessments of the respective scenarios taken from our own daily counseling practice indicated that 481 of all 1488 hypothetical decisions were inappropriate. In 357 cases, necessary postexposure treatment would have been withheld from the individuals seeking advice, whereas in 124 instances, rabies-specific prophylaxis would have been administered or continued in an incorrect way. The resulting overall rate of inadequate advice was about 31% and, thus, almost four times higher among physicians at 11 university-affiliated, urban emergency departments in the United States where within a period of 2 years 173 of 2,030 exposures caused by domestic and wild animals were treated inappropriately.26 The participants of our study were particularly uncertain, for instance, whether or not specific measures should be undertaken in previously vaccinated individuals after exposure to the virus. Consequently, almost 50% of the respondents were not aware that in such cases an abbreviated postexposure scheme is mandatory, regardless of the titer of neutralizing antibodies.7,14–17,27 Similar deficits were encountered concerning a scenario where the necessary postexposure prophylaxis was delayed. Since the extent of a delay that renders treatment ineffective is not known and typical incubation periods of rabies infection range between 1 and 3 months,27 prophylaxis should be started whenever exposure is suspected. A combination of vaccine and rabies immunoglobulin is always recommended in individuals not vaccinated previously and who experienced bites or transdermal scratches, licks on broken skin, or contamination of mucous membranes with saliva. If anatomically possible, the full dose of immunoglobulin should be infiltrated into the wounds and the areas surrounding them. Any remaining volume should be injected intramuscularly at a site distant from vaccine administration.14–17 The assessment of our scenarios finally also demonstrated that problems exist when postexposure prophylaxis had begun abroad and had to be continued after the traveler’s return. These settings sometimes may require both detailed knowledge about rabies vaccines infrequently used or even entirely unknown in some European countries and reliable information on alternative schedules of postexposure prophylaxis.10,16,17,28 As exemplified by the respective casuistry, almost 60% of the participants in our study were not familiar with Verorab®, a modern Vero cell-derived rabies vaccine, which was first introduced in 1985.29 In accordance with the relevant guidelines, they therefore decided to seek further information because they were afraid not only of product falsification and inappropriate storage but also that an obsolete vaccine of nerve tissue origin with a questionable potency and serious side effects30,31 could have been used. Only very experienced travel health advisers were able to make their decision in this situation without further consultations with the manufacturer and knew instantaneously that rabies immunoglobulin that had not yet been given should be administered only during the first 7 days after initiation of vaccination.17,32
Overall, the physicians and pharmacists participating in our survey were well aware of the travel-associated rabies risks and provide information on this health hazard as well as on general preventive measures to the vast majority of their clients who want to visit countries where the disease is enzootic. However, even in this cohort of experienced travel health advisors, evident flaws exist regarding the correct assessment of specific situations in rabies pre- and postexposure prophylaxis. Thus, our study yielded at least some important cues on topics that should be covered more intensely during future postgraduate training in travel medicine and should perhaps also be addressed by more practically orientated recommendations for rabies pre- and postexposure prophylaxis.
The authors are grateful to all physicians and pharmacists who participated in this survey. They are also indebted to the 10 experts in travel medicine who helped to improve the questionnaire, and to Mrs. Delia Cosgrove (Essen University Hospital, Essen, Germany) for editing the manuscript.
Declaration of Interests
The study was funded in whole by Chiron Vaccines, Marburg, Germany, and Mr. Peter Gerold, PhD (Chiron Vaccines, Marburg, Germany) provided comprehensive assistance in conducting the survey.