Determinants of Malaria Prophylaxis Among German Travelers to Kenya, Senegal, and Thailand

Authors


Klaus Stark, MD, PhD, Department of Infectious Disease Epidemiology, Robert Koch Institute, Seestrasse 10, 13353 Berlin, Germany. E-mail: starkk@rki.de

Abstract

Background Malaria chemoprophylaxis is a mainstay of malaria prevention in travelers. Adequate pretravel advice forms the basis for efficient malaria prophylaxis. This study assessed the determinants for seeking pretravel advice and evaluated the quality of advice from each source and its influence on the patterns and outcome of malaria prophylaxis intake.

Methods In March and April 2004, a self-administered questionnaire was distributed by cabin crews to passengers flying back to Germany from three popular tourist destinations: Kenya, Senegal, and Thailand. To evaluate the quality of advice and actual intake, figures were assessed against the official recommendations of the German Society of Travel Medicine and International Health (DTG).

Results A total of 1,001 passengers were included in the study (Kenya, 492; Senegal, 131; and Thailand, 378), of which 81% had sought any kind of pretravel health advice. Travelers’ age and time of pretravel consultation were associated with the source of information consulted. Seventy-five percent of travelers from Senegal and Kenya received DTG compliant advice compared to only 17% of travelers from areas with low malaria risk in Thailand. Travelers returning from Kenya and Senegal had used correct chemoprophylaxis in only 65 and 47% of trips, respectively. In multivariate analysis, the factors determining correct intake among Senegal and Kenya travelers were receiving pretravel advice (from nonmedical professionals: OR 4.4, 95% CI 1.9–10.0 and from medical professionals: OR 15.4, 95% CI 7.3–32.4), a correct risk perception (OR 2.9, 95% CI 1.9–4.5), 2 to 3 weeks of travel abroad (vs a duration >3 wk: OR 2.2, 95% CI 1.3–3.8), and travel to Kenya (OR 1.9, 95% CI 1.1–3.1).

Conclusions Malaria prevention among a large proportion of German travelers to tropical destinations is inadequate. Public health efforts should be made to raise awareness among travelers, travel agencies, and medical institutions in Germany.

Malaria is one of the most important travel-associated diseases due to its widespread geographic distribution and its potential fatal outcome if untreated, especially in nonimmune individuals.1,2 Of the more than 50 million trips abroad made by persons from Germany each year, about 3 to 4 million go to malaria-endemic destinations.3 Germany accounts for around 10% of all reported malaria cases imported to Europe.4–6 Annual notifications ranged between 600 and 1,000 cases (2001–2005), with the highest number of fatal cases being 8 in 2001.7 The majority (>85%) of infections were acquired in sub-Saharan Africa.

Previous studies from different countries showed that between 50 and 90% of travelers to malaria-endemic countries seek any type of pretravel advice.8–15 Such advice is provided by a variety of sources such as institutes and departments for tropical medicine, centers for travel medicine, and local public health offices. In Germany, a high proportion of general practitioners give consultations in travel medicine, and in European countries, many travelers also consult pharmacists and nonmedical sources like travel agents, family and friends, or the Internet.15,16

In addition to bite avoidance and personal protective measures, travelers to endemic areas should take a course of tablets (chemoprophylaxis) to prevent malaria infection. An alternative in low-endemic countries is standby therapy, where travelers can carry a drug abroad, which can be used for emergency self-treatment if fever suggestive of malaria occurs while traveling, and no medical institution can be consulted within 24 hours.

In Germany, the German Society of Tropical Medicine and International Health (DTG) provides regularly updated information on malaria risks and recommendations for prophylaxis.17 Even though the society’s recommendations can be regarded as a formal guideline for travel medicine practitioners, little is known about the quality of country-specific advice on malaria prophylaxis in practice and about the factors that may influence the quality of such advice. The few studies on the quality of pretravel advice showed conflicting results.18,19 Data on the type and accuracy of chemoprophylaxis actually performed by travelers in malaria-endemic countries are particularly scarce because most studies on travel health practices are performed among travelers waiting to depart for tropical countries.12,13,15 In a recent study among German travelers visiting malaria-endemic countries, 20% did not carry any antimalarial drug neither for chemoprophylaxis nor for standby treatment with them.20

We performed a survey among flight passengers returning from Kenya, Senegal, and Thailand to assess the frequency, sources, quality of pretravel advice (according to DTG recommendations), the actual intake of chemoprophylaxis, use of personal protection measures, frequency of carriage and actual intake of standby treatment drugs, and the extent of and reasons for noncompliance. An additional objective was to determine factors (including the source of information) that may influence the quality of travel advice and prophylaxis intake.

Methods

In March and April 2004, a self-administered questionnaire was distributed by cabin crews to all German-speaking passengers flying back to Germany from Mombasa (Kenya, five flights), Dakar (Senegal, six flights), and Bangkok (Thailand, four flights) on board Condor airlines (Condor Flugdienst). The questionnaire covered sociodemographic characteristics, medical history, destination, type of travel, source and type of pretravel advice, recommendations of chemoprophylaxis, intake of and compliance to prophylaxis drugs, carriage and possible intake of standby treatment drugs, personal protection measures, and clinical signs and symptoms of travel-associated diseases. Questionnaires were collected by the airline personnel and sent to the Robert Koch Institute in Berlin. Completed questionnaires from passengers who had stayed at least 24 hours in one of these countries were included in the analysis.

Definitions

Correct advice on malaria prophylaxis was defined as the recommended malaria chemoprophylaxis or carriage of standby medication by destination as described in the national guidelines of the DTG as of 2003.17 Redundant recommendations for chemoprophylaxis, which included the correct drugs plus the carriage of a standby medication, were considered to be correct advice. All travelers to Senegal (apart from those exclusively visiting the Cape Verde Island) and to Kenya were regarded at high risk of malaria. For those, recommended chemoprophylaxis was mefloquine, atovaquone/proguanil, or doxycycline. Thailand was divided into three regions with different levels of risk: high risk (T2), low risk (T1), and no risk (T0) according to DTG standards. High risk applied for the areas near the northwest border to Myanmar (Tak province) and the southeast border to Cambodia (Trat province). The cities Bangkok, Chiang Mai, Chiang Rai, Pattaya, and the Islands Phuket and Ko Samui were regarded as no-risk areas. The rest of Thailand (eg, central region, coast) was defined as a low-risk area. Due to the high proportion of Plasmodium falciparum strains being resistant against chloroquine and mefloquine, standby treatment only with atovaquone/proguanil or artemether/lumefantrine is recommended by DTG for T1 areas and continuous prophylaxis with atovaquone/proguanil or doxycycline for T2 areas.

Data processing and statistical analysis

The data were entered into an MS Access database by scanning the questionnaires with the help of Forms5 software (ReadSoft AB, Helsingborg, Sweden). A set of 44 consecutive questionnaires with 182 cross and numeric fields each from one of the batches in the middle of the study period were selected to check the scanner results with the original filled-out questionnaires. Data were analyzed with SPSS (version 14.0 for Windows; SPSS Inc., Chicago, IL, USA). Multivariable analysis was performed using logistic regression models with stepwise forward selection of variables. Variables were included in the model when univariate analysis showed a significant association with the outcome (p < 0.05) and remained in the model on the basis of the likelihood ratio statistic (p < 0.05).

Results

Study population

During 15 flights to Germany, a total of 1,364 questionnaires were distributed to German-speaking adults, of which 1,030 (76%) were returned to the cabin crew. Overall, 1,001 (97%) travelers fulfilled the entry criteria and were included in the analysis. Of these, 492 (49%) returned from Kenya, 131 (13%) from Senegal, and 378 (38%) from Thailand. Fifty-two percent were males, and 95% were of German nationality. The median age was 47 years (range 18–79). The purpose and duration of travel as well as the type of accommodation are listed in Table 1.

Table 1.  Frequencies (%) of characteristics and travel profile of study participants
 Kenya (n = 492)Senegal (n = 131)Thailand (n = 378)Total (n = 1,001)p
  1. ns = not significant (p value > 0.05); VFRs = visiting friends or relatives.

Age group (y) (n = 993)
 18–3929.932.028.731.1ns
 40–5945.147.751.246.9 
 60+25.020.320.122.0 
Sex (n = 989)
 Male48.744.258.751.90.002
 Female51.355.841.348.1 
Residence (n = 896)
 West Germany67.390.183.876.5<0.001
 East Germany32.79.916.223.5 
Purpose of travel (n = 990)
 Leisure87.072.380.382.6<0.001
 Backpack7.24.06.46.5 
 VFR2.019.06.45.9 
 Expatriate2.31.64.02.8 
 Other business1.43.22.92.2 
Accommodation (n = 995)
 Hotel89.065.988.085.6<0.001
 Apartment5.110.95.96.1 
 Family2.722.54.05.7 
 Tent, camping2.90.80.81.8 
 Others0.401.30.7 
Duration (d) (n = 983)
 ≤1423.337.517.122.8<0.001
 15–2153.239.853.251.5 
 >2123.522.729.725.7 

Pretravel advice

Of all participants, 81% had sought any kind of pretravel health advice (Kenya 89%, Senegal 82%, and Thailand 70%). The main sources of advice (n = 769) were general practitioners (48%), followed by tropical medicine institutes (22%), public health offices (9%), friends or family (6%), the Internet (5%), pharmacies (4%), travel agencies (4%), and others (2%). The majority of travelers (55%) obtained pretravel health advice 1 to 6 weeks before departure and 7% within the 7 days before departure. Timing of travel advice and age group had significant influence on the use of sources: last-minute advice seekers (<7 d before departure) and travelers below 40 years of age sought pretravel advice from nonmedical sources more often than other travelers (36% vs 17% and 39% vs 30%, respectively, for both p < 0.03). The main reasons for not seeking advice (n = 191) were that individuals considered themselves sufficiently informed (70%) or that they perceived no risk at their destination (overall 16%; Kenya 7%, Senegal 19%, and Thailand 20%). The proportion of travelers seeking pretravel advice did not differ by purpose of travel [travelers visiting friends or relatives (VFRs), 67%; tourist travelers, 70%; and expatriates, 77%].

Travelers to Kenya and Senegal

Risk perception

Of all travelers to Kenya or Senegal, less than half (43%) correctly perceived the risk of malaria as high (Kenya 45% vs Senegal 35%, p < 0.001), 45% considered it to be low, 2% perceived no risk, and 10% could not classify the risk. Travelers with pretravel advice were significantly more likely to correctly perceive a high risk than travelers without any pretravel advice (51% vs 32%, p = 0.006).

Recommendations for malaria chemoprophylaxis

For both the Kenya travelers (n = 402) and the Senegal travelers (n = 85) with a prophylaxis recommendation, 91% had a recommendation for continuous prophylaxis and 9% for standby medication only. The drugs recommended for continuous intake were mefloquine (65%), atovaquone/proguanil (33%), and doxycycline (2%) (multiple response possible). However, chloroquine was recommended in 5% of travelers to either one of the two countries (2% alone and 3% in combination with proguanil, total of n = 18 travelers). Twenty-two travelers were not able to recall their drug recommendation. No significant differences between Kenya and Senegal travelers were found.

If advice was given for standby medication only (Kenya 36 travelers and Senegal 8 travelers), the most frequently recommended drug was mefloquine (43%) followed by atovaquone/proguanil (27%). Chloroquine was recommended for standby treatment in six Kenya travelers (in 11% as monotherapy and in 2% in combination with proguanil). Other answers were “don’t know the medication” (21%) and “other” (2%).

Overall, in 76% of Kenya travelers (313/411) and in 70% of the Senegal travelers (64/92), pretravel chemoprophylaxis recommendations were DTG compliant (Table 2). Chemoprophylaxis recommendations for Kenya and Senegal travelers were likely to be DTG compliant if they were provided by medical professionals: public health services (91%) and tropical medicine institutes (83%) (Figure 1). Table 3 shows additional variables found to be associated with the correctness of chemoprophylaxis recommendations for travelers obtaining pretravel advice (n = 503). DTG compliant recommendations were more frequently provided to travelers with a shorter (<21 d) duration of stay abroad (p = 0.02), to those who consulted medical professionals (p< 0.001), and to those who received advice between 6 weeks and 6 months before starting the journey (p = 0.04). In multivariable analysis, the source of information remained significantly associated with correct advice. Travelers who had consulted institutions with medical professionals were almost four times more likely to receive correct advice (OR 3.9, 95% CI 2.2–6.8) compared to those who obtained their pretravel information from other sources.

Table 2.  DTG compliant recommendations and correct prophylaxis intake in travelers visiting Kenya and Senegal
 Kenya (n = 492)Senegal (n = 124)Total (n = 616)
  • DTG = German Society for Tropical Medicine and International Health.

  • *

    This includes also non-DTG compliant antimalarial drugs (eg, chloroquine).

  • For percentage, travelers with missing data excluded.

Travelers without pretravel advice54 (11.0)23 (18.5)77 (12.5)
Travelers with pretravel advice438 (89.0)101 (81.5)539 (87.5)
 Type of advice (% of travelers with advice)
  Continuous chemoprophylaxis*366 (83.6)77 (76.2)443 (82.2)
  Standby treatment advice only36 (8.2)8 (7.9)44 (8.2)
  None9 (2.0)7 (6.9)16 (3.0)
  Unknown23 (5.3)8 (7.9)31 (5.8)
  Data missing4 (0.9)1 (1.0)5 (0.9)
 DTG compliant advice313 (76.2)64 (69.6)377 (75.0)
Correct intake
 Among all travelers (% of all travelers)308 (65.1)54 (47.4)362 (61.7)
 Among travelers with advice (% of travelers with advice)
  After DTG compliant advice285 (91.9)50 (78.1)335 (89.6)
  After non-DTG compliant advice14 (14.3)2 (7.1)16 (12.7)
 Among travelers without pretravel advice8 (14.8)2 (11.8)10 (14.1)
Figure 1.

Accuracy of recommendations on malaria chemoprophylaxis for Kenya and Senegal by main source of travel advice (n = 470).

Table 3.  Variables associated with factors determining DTG compliant prophylaxis recommendations by advice and correct intake in travelers visiting Kenya and Senegal
VariablesCorrect DTG recommendation (n = 503), % totalp ValueCorrect intake (n = 587), % totalp Value
  1. VFRs = visiting friends and relatives; DTG = German Society for Tropical Medicine and International Health.

Countryn = 503 n = 587 
 Kenya76.2ns65.1<0.001
 Senegal69.6 47.4 
Residencyn = 449 n = 523 
 Former West Germany72.40.02960.9ns
 Former East Germany82.1 68.0 
Purpose of traveln = 498 n = 580 
 Leisure, backpack75.3ns63.40.008
 VFR65.5 50.0 
 Others (eg, expatriate, business)73.3 34.8 
Type of accommodationn = 501 n = 586 
 Hotel, tent, boat76.2ns65.0<0.001
 Apartment, family/friends66.7 40.0 
Duration of journey (d)n = 493 n = 577 
 <1476.60.01957.4<0.001
 14–2178.3 69.4 
 >2164.4 50.4 
Source of advicen = 495 n = 483 
 Medical81.7<0.00175.5<0.001
 Nonmedical49.4 46.2 
Time of advice seekingn = 479 n = 488 
 >6 mo before64.30.04249.3<0.001
 6 wk to 6 mo before82.8 74.4 
 1 and 6 wk before76.2 74.5 
 <7 d before75.0 55.2 
Recommendation DTG compliant n = 504 
 Yes 89.6<0.001
 No 12.7 
Subjective risk perceptionn = 458 n = 536 
 Correct81.9<0.00175.3 
 Incorrect66.1 48.0<0.001

Chemoprophylaxis intake

A total of 66% travelers reported continuous intake of chemoprophylaxis: 69% in Kenya and 53% in Senegal (p = 0.001). Overall, DTG compliant drug intake was reported by 62% of all travelers to Kenya and Senegal (65% vs 47%, respectively, p < 0.001) (Table 2). Of those with DTG compliant prophylaxis advice, 90% correctly took the chemoprophylaxis compared to only 13% of the travelers with inadequate chemoprophylaxis advice and 14% of persons without any pretravel advice (Table 2). The main reasons for not taking chemoprophylaxis where recommended (n = 56 answers available) were fear of adverse events (52%), previous experience of adverse events (25%), and “no risk perceived” (29%). Of the persons who considered themselves sufficiently informed and did not seek travel advice, only 18% (10/55) took the correct prophylaxis. Deviations from the recommended regimen, eg, by taking other drugs, dosages, or intake duration as recommended, were found in 8% of the Kenya travelers and in 21% of the Senegal travelers.

Drugs taken for chemoprophylaxis were mefloquine (63%), atovaquone/proguanil (30%), doxycycline (2%) but also chloroquine (3%) and chloroquine/proguanil (3%).

Overall, 9% (n = 32) of the Kenya and Senegal travelers stopped taking their chemoprophylaxis before the recommended date. The main reasons for noncompliance were “absence of mosquitoes” (53%) and “adverse events” (22%). Among the total 209 travelers visiting Kenya or Senegal without continuous drug intake, 57 reported to have received a recommendation to carry a standby medication (88 without any recommendation and 64 with missing value), of which 64% actually carried the drug abroad.

Table 3 shows variables (in addition to the variable “DTG compliant pretravel advice”) that were associated with correct intake. In multivariable analysis, independent factors associated with correct chemoprophylaxis drug intake were travel to Kenya, pretravel advice from a medical professional, duration of stay abroad 15 to 21 days, and correct malaria risk perception (Table 4).

Table 4.  Multivariate analysis of factors determining correct antimalarial chemoprophylaxis intake for high-risk sub-Saharan countries Kenya and Senegal
Variables*OR95% CIp Value
  • *

    Destination: Kenya (1) versus Senegal (0); pretravel advice: medical professional (2), nonmedical (1), no advice at all (0); duration of journey: >21 days (0), ≤14 days (1), 15 to 21 days (2); and malaria risk perception appropriate: yes (1) versus no (0).

Destination
 Senegal1.00
 Kenya1.851.10–3.110.021
Source of advice
 No advice at all1.00
 By nonmedical   professional4.361.89–10.06<0.001
 By medical   professional15.397.30–32.44<0.001
Duration of travel (d)
 >211.00
 15–212.211.29–3.770.004
 ≤141.270.71–2.320.404
Risk perception  correct: yes vs no2.911.89–4.50<0.001

Travelers to Thailand

Of all 378 Thailand travelers, 86% stayed in areas with a low malaria risk (T1, n = 325) and 13% in areas without any risk (T0, n = 49). Two persons traveled to high-risk areas (two travelers visited unknown areas).

Risk perception

The majority of travelers to Thailand perceived the risk of malaria at their destination correctly (71%). For low-risk areas, this was true for 79%, whereas 13% had no risk awareness and 7% overestimated the risk. For no-risk areas, risk assessment was correct for 21%, but most travelers overestimated the malaria risk (72% low risk and 6% high risk). One of the travelers to high-risk areas perceived only low risk and the other no risk at all.

Chemoprophylaxis recommendations and intake

In total, 276 travelers (70%) had sought pretravel advice, 73% of those visiting areas with a low malaria risk and 55% of travelers to areas without malaria risk. One of the two high-risk area travelers reported having obtained travel advice. Of the 237 participants with pretravel advice traveling to low-risk areas, 43% (99/232 respondents) received a recommendation for chemoprophylaxis or standby treatment: 12% chemoprophylaxis only, 6% chemoprophylaxis plus standby treatment, and 25% standby treatment only. Recommended drugs for chemoprophylaxis or standby were atovaquone/proguanil (30%, 46%), mefloquine (34%, 28%), doxycycline (7%, 5%), chloroquine/proguanil (9%, 3%), and chloroquine alone (7%, 4%) (don’t know: 13%, 14%). More than half of the travelers to low-risk areas received no recommendation for prophylaxis (56%). Overall, only 37 (17%) of 215 travelers to T1 areas with available information received a DTG compliant recommendation.

Among the participants with pretravel advice for no-risk areas, 64% (16/25) were correctly counseled that malaria prophylaxis was not necessary. The traveler to the high-risk areas was advised to take continuous prophylaxis.

Of the 315 travelers to low-risk areas in Thailand with pretravel advice, 6% took chemoprophylaxis (although not recommended by DTG) and 57% carried a standby medication. Of the travelers reporting a recommendation for standby (n = 72), 68% carried an antimalarial drug abroad.

Personal protection measures against mosquito bites

Among Kenya and Senegal travelers, the majority (78%) reported to have applied one or more preventive measure against mosquito bites. Measures (for Kenya n = 415 travelers and Senegal n = 101 travelers) included the use of mosquito nets (68 and 65%), insect repellents (75 and 59%), clothes completely covering arms and legs (50 and 48%), and use of impregnated clothes/mosquito nets (9 and 12%). Twenty-eight percent of these high-risk travelers used both personal protection measures and correct chemoprophylaxis. There was no association between correct personal protection measures and antimalarial chemoprophylaxis: 45% of travelers with correct chemoprophylaxis also used adequate personal protection measures against exposure compared to 41% of those without correct chemoprophylaxis (p = 0.36).

Among Thailand travelers, one or more personal protection measures were applied in 57% while visiting low-risk areas (T1) and in 69% while visiting no-risk areas (T0). Among travelers with answers (n = 299), personal protection measures consisted of the use of mosquito nets (T1 23% and T0 19%), insect repellents (74 and 79%), clothes completely covering arms and legs (45 and 43%), and impregnated net/clothes (5 and 10%). During pretravel advice, recommendations on personal protection measures were received by travelers with standby treatment advice in 44% (58/133).

Health problems and standby medication for travelers to Kenya, Senegal, and Thailand

Of all travelers, 27 (3% of n = 942 respondents) felt feverish during their journey: 11 in Kenya, 9 in Thailand, and 7 in Senegal. Ten reported a self-measured temperature of 38°C and more. Of the 20 feverish patients who responded to the question, 12 were taking continuous chemoprophylaxis.

Of all 27 febrile travelers, 6 visited a physician to rule out malaria. Malaria was confirmed in one patient visiting Senegal who did not take continuous chemoprophylaxis. In total, five persons took a self-treatment (three with fever and two without fever). Seven febrile travelers reported having carried standby medication but did not use it for self-treatment according to the following reasons: temperature fell after using another treatment (n = 3), temperature fell by itself (n = 3), and belief that the temperature was not dangerous (n = 1).

Discussion

Malaria can effectively be prevented by using antimalarial drugs for continuous chemoprophylaxis. In our study, however, only 65% of travelers to Kenya and 47% of travelers to Senegal had used correct chemoprophylaxis. These figures are disturbingly low, even if one takes into account inaccurate recall in some participants and the fact that a few travelers stayed only for a couple of days.

Malaria was the most frequent cause for systemic febrile illness among ill-returning travelers reported to the surveillance system GeoSentinel (352 cases per 1,000 febrile patients).21 Data from 3,752 German travelers reported with falciparum malaria between 1993 and 2004 showed that 60% did not take any chemoprophylaxis. If malaria occurred despite chemoprophylaxis, the intake was still able to significantly reduce fatality rates.22 These figures underline the importance of continuous chemoprophylaxis in travelers visiting high-risk areas, especially in sub-Saharan Africa.

Our study highlights two important steps in advance of actual drug intake that contributed to this situation of inadequate malaria prophylaxis: determinants seeking pretravel advice and receipt of correct recommendations during this advice. We found that good advice was the strongest predictor for good intake practice. Of all 149 travelers in high-risk areas without accurate intake, three quarters had not obtained accurate advice prior to their trip.

Among travelers without pretravel advice, usage of correct chemoprophylaxis was particularly poor. Besides the fact that these individuals considered themselves already sufficiently informed, perceiving no risk at their destination was the predominating reason for not seeking advice. Previous studies identified VFRs as a risk group seeking pretravel advice less often than tourist travelers.23–25 Among 5,067 passengers surveyed at European airports prior to departure, only 31% of VFRs had sought pretravel advice compared to 61% of tourists.15 Probably as a consequence, immigrant VFRs were found in another study to be four times more likely to receive a diagnosis of malaria than did tourist travelers.25 In our study, VFRs did not seek pretravel advice significantly less often (67%) when compared to tourist travelers (77%). Regarding chemoprophylaxis intake, however, VFRs were significantly less likely to use correct chemoprophylaxis than other groups. Possible explanations for this discrepancy could be barriers due to the cost of the drugs or beliefs to be somehow not at personal risk.26 Overall, the validity of perceived risk for malaria among travelers to Senegal and Kenya was surprisingly low at 43% but higher in travelers visiting Thailand (71%). The findings of the European Airport Study were different: 77% of travelers visiting high-risk malaria-endemic areas perceived the risk as high, while only 40% of travelers visiting low-risk areas perceived the risk as low.15 In our study, correct risk perception was associated with a higher frequency of correct chemoprophylaxis intake but not with a higher frequency of performed preventive measures against mosquito bites.

The quality of received advice was assessed by comparing it to the official recommendations of the DTG. Of those travelers to the African countries with pretravel advice, the vast majority (Kenya 93% and Senegal 85%) received a recommendation for chemoprophylaxis or at least standby treatment. However, the recommended chemoprophylaxis did not concur with the official guidelines in a significant proportion of travelers. Thus, the quality of pretravel advice should be improved in addition to improving the percentage of travelers who receive advice. Overall, travelers were significantly more likely to receive correct chemoprophylaxis recommendations if they consulted medical sources. Recommendations provided by public health offices were most often in accordance with DTG guidelines, followed by institutes of tropical medicine. A reason for the slightly lower frequency of DTG compliant advice at tropical institutes might be that these institutions with broad expertise in travel medicine tailored the advice according to the needs and characteristics of the individual traveler. As a consequence, their advice could differ from DTG standard recommendations but still may be correct after taking into account duration, purpose, and route of the journey.27

Recommendations by pharmacists were with 70% accuracy for Kenya, the best of all nonmedical sources, comparable with a previous observation among Swiss pharmacists with 74% accuracy for Kenya.28 Interestingly, half of the travelers using the Internet as the main source reported accurate recommendations, which is unexpectedly high compared with other recent studies on the quality of travel health on the Web.29,30

Of the travelers with accurate recommendations, 10% failed to take the prophylaxis mainly because of fear of adverse events. In recent studies, this reason for noncompliance was also observed.31,32 Furthermore, participants traveling longer than 3 weeks were more than twice as likely to take incorrect or no drugs compared to those traveling 2 to 3 weeks. For long-term travelers, individually tailored malaria prophylaxis schemes (rather than strictly standardized recommendations) should be provided by travel medicine experts.33

Noncompliance with chemoprophylaxis once started appears to be another substantial problem among travelers: travelers visiting Kenya and Senegal admitted to have ceased the prophylaxis intake too early in 10 and 20%, respectively. An even lower adherence to chemoprophylaxis was observed in a study among adult travelers to sub-Saharan Africa using electronic monitoring.34 Interestingly, absence of mosquitoes was the most frequently self-reported reason for noncompliance (50%) followed by adverse events in only 22% (independent on the source of pretravel advice). It seems that more education is needed regarding the fact that not observing mosquitoes does not mean no risk of malaria. Furthermore, behavior in case of febrile illness has to be improved: only 22% of travelers with fever consulted a health practitioner to rule out malaria.

Thailand is a country with areas of no or low risk for malaria but with high risk in border areas to Burma and Cambodia. This fact seems to make correct (DTG compliant) advice more difficult: almost 20% of travelers visiting low-risk areas received the recommendation for continuous chemoprophylaxis during pretravel advice consultation and only 25% received the correct advice to carry a standby medication only. Nonetheless, malaria is transmitted in Thailand, and the reemergence of the disease in some southern parts of the country led recently to infections in two travelers from Israel and in one German traveler.35,36

A few limitations of our study have to be considered. In some travelers, there was a considerable time period between the advice prior to travel and the completion of the questionnaire at the end of the trip, which might have introduced recall problems. The response rate of 73% among the flight passengers fulfilling the inclusion criteria was high. Nevertheless, the proportion of correct chemoprophylaxis intake among those nonparticipating travelers is likely to be lower than in travelers interested in filling out the questionnaire. Thus, the true frequency of correct intake might have been even worse than calculated from the questionnaires we received.

In conclusion, this present study shows that medical background of the pretravel health information source and correct travelers’ risk perception are the most important determinants for both DTG compliant recommendation and correct intake. The study has significant implications for improved pretravel advice to reduce malaria risks for travelers to popular tourist destinations. First, it is necessary that more travelers receive adequate pretravel advice. Travel agencies may play a pivotal role to motivate their clients to seek travel advice from competent institutions and experts in travel medicine on time. Public health campaigns concerning travelers’ health would also contribute to better malaria prophylaxis and immunization coverage among travelers. Second, the quality of pretravel advice concerning malaria chemoprophylaxis should be improved. Whereas the information obtained from medical sources is generally of high quality, there should be efforts to raise the standards of malaria prophylaxis recommendations provided by nonmedical sources. Additional training in travel medicine for general practitioners is also warranted.

Acknowledgments

We thank Ms Froese (Lufthansa) and Ms Roshan-Moniri (Condor Flugdienst GmbH of Lufthansa Airlines, Medical Service, Frankfurt, Germany) for their logistic support of this study. No financial support was received for the study.

Declaration of interests

The authors state that they have no conflicts of interest.

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