The number of people, both adults and children, traveling abroad, is on the rise. Some seek counseling at travel medicine centers before departure.
The number of people, both adults and children, traveling abroad, is on the rise. Some seek counseling at travel medicine centers before departure.
A prospective study was conducted among children <16 years visiting a travel medicine center in Marseille, France, from February 2010 to February 2011. Parents were contacted by telephone 4 weeks after their return, and asked about compliance with pre-travel advice.
One hundred sixty-seven children were evaluated after their trip. Compliance with immunizations, malaria chemoprophylaxis, and food-borne disease prevention was 71, 66, and 31%, respectively. Compliance with malaria chemoprophylaxis varied significantly with destination, and was higher for African destinations. Significant features associated with poor compliance with chemoprophylaxis were a trip to Asia or the Indian Ocean, age <5 years, and a monoparental family. Compliance with prevention of food- and water-borne diseases was higher in children < 2 years of age.
A ≥80% compliance with pre-travel counseling in children traveling overseas was achieved only for drinking bottled water, using repellents, a routine vaccine update, and yellow fever immunization.
In France, it is estimated that half a million children travel to the tropics annually. Their main purpose of travel is tourism, but some of them are visiting friends and relatives (VFR) abroad with their caregivers. Travel medicine centers provide authentic information[3, 4] and health education to families regarding travel-related risks and their preventive measures. Compliance with pre-travel advice has never been well evaluated in families with children. This 1-year prospective study, conducted in a travel medicine center in southern France, aimed to report pediatric data on compliance with the prophylactic measures.
The study took place in the Marseille Travel Medicine Center located in a tertiary university hospital in southern France (CHU Nord, Marseille) from February 2010 to February 2011. It was approved by the Ethical Committee of the Marseille Faculty of Medicine. During the stated period, the center counseled more than 3,800 travelers. Families with children under 16 years of age seeking advice before a journey to the tropics were invited to take part in the study. “Tropics” included sub-Saharan Africa and Indian Ocean islands, Southeast Asia and India, and Central and South America. Written parental consent was obtained for a telephone-based questionnaire which would be completed on their return. People traveling for more than 3 months were excluded, as they were likely to be unattainable by telephone, and were less likely to remember all the preventive measures that they had been advised to take. Moreover, people living abroad for a very long time frequently relax preventive measures, which could introduce bias into the study.
Information on baseline demographics, type of journey, and children's previous vaccines was obtained. Children VFR were defined as persons returning to their homeland to visit friends or relatives (even if born in the country of residence or from different parental origins). The discussion focused on travel-associated risks and their prevention. Routine vaccination updates and specific immunizations were recommended according to risk. Depending on the risk of malaria and specific contraindications, chemoprophylaxis and protective measures against mosquitoes were prescribed.[8-10] Prevention and self-treatment of travel-related diarrhea were explained. Families were given a standardized written information document, summarizing the main risks (malaria, diarrhea, injuries, sunburn, etc.) and their prevention. They also received an order form for a standardized pediatric medical kit.
Parents were contacted by telephone 4 weeks after their return for a post-travel questionnaire. This interval was chosen to assess full compliance with malaria chemoprophylaxis. The standardized questionnaire recorded data relating to compliance with pre-travel advice and lasted around 5 minutes per child.
Data were anonymized. The statistical software Stata 7.0 (Stata Corporation College Station, TX, USA) was used. The effect of categorical covariates was tested using chi-square or Fisher's exact tests, whereas quantitative covariates were compared using Student t-test and analysis of variance. All tests and confidence intervals were two-sided with a p = 0.05 alpha risk.
In order to assess the effects of covariates upon the therapeutic compliance with malaria chemoprophylaxis, we took in account that (1) only a few children received chloroquine ± proguanil or doxycycline, (2) in these children, the prescription could be related to specific travel conditions: for chloroquine ± proguanil, low prevalence of drug resistance in the area of travel (ie, the destination of the trip) or weight <10 kg (contraindicating atovaquone-proguanil or mefloquine in France), and for doxycycline, age >8 years. Only eligible children treated with atovaquone-proguanil or mefloquine were consequently included in the analysis of factors associated with compliance. A multivariate model (logistic regression analysis with clustered data) was then built. It was chosen because of the assumption (considered strong enough) of a nonindependent behavioral within each family with regard to risk managing and compliance. Variables with p < 0.1 in univariate analysis were candidates for inclusion in the multivariate analysis.
During the period, 185 children (122 families) attending the center for pre-travel advice agreed to participate. One hundred sixty-seven (90%) children (109 families) were evaluated by the post-travel questionnaire. Three (2%) children had cancelled their journey and 15 (8%) were unobtainable for follow-up. Sex ratio was 1.0 and mean age 68 (SD = 54) months. Ninety-nine (54%) children traveled to Africa, 48 (26%) to Indian Ocean, 18 (10%) to Asia, and 20 (11%) to South America. The five most visited countries were the Comoros (22%), Senegal (18%), Kenya (8%), Cameroon (7%), and French Guyana (5%). The mean duration of travel was 29 days (SD = 19). One hundred eighty-three (99%) children were born in France, but only 103 (56%) had European maternal ascendance. Thirty-seven (20%) of the children lived with only one of the parents (monoparental families) and 41 (22%) children had state health insurance.
One hundred two children (55%) were VFR and 83 (45%) were traveling for tourism. As shown in Table 1, VFR children significantly differed from tourists in age (younger), maternal origins (outside Europe), family structure (monoparental), health insurance (state insurance), siblings (higher number), destination (Indian Ocean), housing during travel (local housing), duration of the stay (longer), and time between pre-travel visit and departure (shorter).
|VFR children||Tourist children||Odds ratio||p-Value|
|n = 102 (%)||n = 83 (%)||[95% CI]|
|Mean (months, SD)||43 (43.0)||99 (50.0)||<0.0001|
|<5 years||72 (70.6)||18 (21.7)||8.7 [4.4–18.0]||<0.0001|
|Mother born outside Europe||76 (74.5)||7 (5.4)||31.7 [13.0–77.5]||<0.0001|
|State health insurance||38 (37.3 )||3 (3.6)||15.8 [4.16–60.3]||<0.0005|
|Monoparental family||28 (27.5)||9 (10.8)||3.1 [1.4–7.0]||0.005|
|≥3 children at home||45 (44.1)||20 (24.1)||2.5 [1.4–7.0]||0.005|
|Africa||51 (50.0)||48 (57.8)||1||<0.0005|
|Asia||1 (1.0)||17 (20.5)||0.06 [0.01–0.49]|
|Indian Ocean||43 (42.2)||5 (6.0)||8.09 [2.73–24.0]|
|South America||7 (6.9)||13 (15.7)||0.51 [0.18–1.39]|
|Local housing during travel (urban and/or rural housing)||102 (100.0)||53 (63.9)||Not calculable||<0.0001|
|Duration of travel|
|Mean duration (days, SD)||40 (18.0)||17 (8.0)||<0.001|
|>15 days||92 (90.2)||29 (34.9)||17.1 [7.75–37.9]||<0.0001|
|Mean time between pre-travel visit and departure (days, SD)||32 (23.0)||45 (30.0)||<0.0001|
Table 2 reports the compliance with prophylactic measures among the 167 post-travel evaluated children.
|Prophylactic measures||Number of compliant children (%)a|
|Immunizations (really done/proposed during visit)|
|– Routine vaccines update||60/74 (81.1)|
|– Yellow fever||94/94 (100.0)|
|– Hepatitis A||85/114 (74.6)|
|– Typhoid fever||46/60 (76.7)|
|– Bacillus Calmette Guerin||9/25 (36.0)|
|Full compliance with all recommended vaccines||118/167 (70.7)|
|Malaria chemoprophylaxis (fully compliant children/children using the chemoprophylaxis)|
|– Atovaquone-proguanil||51/70 (72.9)|
|– Mefloquine||38/57 (66.7)|
|– Doxycycline||6/15 (40.0)|
|– Chloroquine||2/3 (66.7)|
|– Chloroquine-proguanil||0/2 (0)|
|Compliance with antimalarials|
|– Antimalarials purchased by parents||136/147 (92.5)|
|– Correct intake during travel||121/147 (82.3)|
|Adequate compliance during and after travel||97/147 (66.0)|
|Protection against arthropods bites|
|– Use an insect repellent||140/147 (95.2)|
|– Use a bed net||104/147 (70.7)|
|– Use insecticides||80/147 (54.4)|
|Use of insect repellent, bed net, or insecticides||147/147 (100)|
|Food and water|
|– Do not drink tap water||133/167 (79.6)|
|– Do not eat uncooked vegetables or salads||82/167 (52.7)|
|– Do not use ice cubes nor eat ice creams||121/167 (72.5)|
|– Do not buy food sold in the street||113/167 (67.7)|
|Safe food and drinking water only||51/167 (30.5)|
Only 75 (41%) children were already fully immunized with routine vaccines. Differences were observed in vaccine coverage: 84% for diphtheria, tetanus, poliomyelitis, pertussis, or Haemophilus influenzae type B, but 54% for hepatitis B.
A routine vaccine update and travel-specific vaccines were proposed to 74 (40%) and 132 (71%) children, respectively. Among the 167 children for whom vaccination was recommended, 118 (71%) were fully compliant. Yellow fever vaccine was accepted in 100% of cases. Acceptance rates of hepatitis A, typhoid fever, and Bacillus Calmette Guérin immunizations were 75, 77, and 36%, respectively. Parents' reasons for not going ahead with prescribed vaccinations (49 children) were: cost of vaccines (12%), fear of adverse events (12%), neglect of vaccination (6%), perceived inefficacy of vaccines (4%), or lack of time before departure (2%).
One hundred sixty-one (87%) children were prescribed antimalarials: atovaquone-proguanil (46%), mefloquine (40%), doxycycline (9%), chloroquine (2%), and chloroquine plus proguanil (2%). Of those children 147 (91%) were evaluated on their return. All had used at least one form of protection against arthropod bites (repellent 95%, bed net 71%, or insecticides 54%) but only 46 (31%) children had used the three types of protection. The chemoprophylaxis was purchased for 136 (93%) children. One hundred twenty-one (82%) children regularly took the drug (full compliance) during the trip, and 97 (66%) continued to do so on their return. Chemoprophylaxis was discontinued for side effects in 19 (13%) children. The reported side effects for atovaquone-proguanil, mefloquine, doxycycline, and chloroquine (with or without proguanil) were 13 (19%), 3 (5%), 2 (13%), and 1 (20%), respectively (p = 0.09). Compliance rates relating to atovaquone-proguanil and mefloquine, the most frequently used prophylaxis, were similar (73% vs 67%, p = 0.56). Compliance significantly varied with destination, whatever the drug (South America 29%, Indian Ocean 44%, Asia 62%, and Africa 80%, p < 0.0005).
Independent variables significantly associated with low compliance relating to atovaquone-proguanil or mefloquine (Table 3) were age <5 years, destination (Indian Ocean and Asia), and monoparental family. Compliance was identical between VFR and tourist children, irrespective of the duration of the trip or the type of chemoprophylaxis.
|OR||[95% CI]||p||aOR||[95% CI]||p|
|Age < 5 years||2.97||[1.34–6.56]||<0.01||3.19||[1.09–9.34]||0.03|
|Mother born outside Europe||2.02||[0.94–4.38]||0.08||1.20||[0.31–4.65]||0.79|
|State health insurance||2.29||[0.89–5.89]||0.12||—|
|– Indian Ocean||5.76||[2.30–14.4]||3.27||[0.91–11.7]|
|– South Americaa||∞||[0.0–∞]||—|
Parents reported full compliance with all the measures to minimize food- and water-related diseases for only 51 (31%) children. Eighty percent of the children did not drink tap water, but other recommendations regarding food preparation and consumption were less frequently respected. Families were significantly more compliant with all recommended measures if the child was under 2 years in univariate analysis (OR = 4.38 [2.15–8.94]). VFR status, maternal age, familial features, health or travel insurance status, and duration of stay were not associated with greater compliance after adjustment (data not shown).
This prospective study is the first in France to evaluate compliance of children traveling overseas after counseling at the travel medicine center. The principal outcome of the study is that compliance ≥80% was achieved for routine vaccine updates, yellow fever immunization, the use of repellents, and drinking bottled water, solely. Other measures were less frequently followed.
As shown, an appointment at a travel medicine center is an opportunity to update routine vaccinations. The overall 71% compliance with vaccines may be related to the fact that the yellow fever vaccine (compliance 100%) is sometimes mandatory and also only available in travel medicine centers in France. As some parents visited the center for this vaccination, they might have accepted the other immunizations more easily. Compliance with hepatitis A and typhoid vaccines was also close to 75%, higher than compliance reported in another study recently conducted in adults traveling overseas.
The 66% malaria chemoprophylaxis compliance is consistent with other studies.[12-14] Reasons previously reported for poor compliance are destination[15, 16] and young age[14, 17, 18] (as in our patients), as well as purpose of the trip (VFR or tourism) and malaria prophylaxis tolerance (neither significant in this study). In fact, VFR people are an extremely varied group. A recent French national study reported that the socioeconomic and educational level of direct descendants of immigrants is intermediate between immigrants themselves and French natives. In the study, VFR children were mainly born in France (second or third generation immigrants). We speculate that their families were probably quite well assimilated, and, for this reason, might be more likely to take preventive measures.
Financial considerations have to be taken into account for preventive measures, as reflected by the 13% of children that did not buy atovaquone-proguanil, the most expensive drug, after counseling (data not shown). Malaria chemoprophylaxis is not refunded by the French national health system or by personal health insurance, and preventive treatment has to be paid for by families themselves. Monoparental status has already been associated with poor compliance with common vaccines. It is frequently associated with low income, which could explain the lower compliance with chemoprophylaxis reported in this group.
Finally, we cannot rule out the possibility that certain chemoprophylaxis were disrupted because they were not in accordance with the local profile of malaria in the region visited. In Southeastern Asia especially, transmission may vary within a country, from one area to another. When the local epidemiology is not well known, some practitioners may overprescribe chemoprophylaxis just to be safe.
It is common for travelers to disregard dietary recommendations.[12, 24] However, most parents reported drinking bottled water. As in other studies, families with young children were also the most compliant with advice relating to food and water.
There are certain limitations that need to be acknowledged regarding this study. To minimize recall bias, families were contacted shortly after their return, but children were invited to join the study before departure. We cannot rule out the possibility, therefore, that knowledge of inclusion in a preventive study meant that the measure of compliance was probably higher than it might otherwise be. Furthermore, parents seeking care in a travel medicine center before departure probably worry about travel-related diseases more frequently than others, and they may be more compliant. For instance, the compliance with hepatitis A vaccination was higher in our study than in another French one taking place in mother and infant welfare services. Our children are probably not representative of all children traveling abroad either. We speculate that families with poor language skills, or those poorly assimilated into French culture, for instance, do not readily visit a travel medicine center before a “tropical” journey. In our pediatric experience, they would rather visit a general practitioner closer to their residence, or travel without any counseling.
The prevention of travel-related diseases in children traveling abroad depends on the ability of the family to maintain high levels of compliance before and after the trip. In our children, full compliance with the vaccines offered, malaria chemoprophylaxis, and food- and water-related disease prevention were 71, 66, and 31%, respectively. Compliance reached ≥80% for the consumption of bottled water, the use of repellents, routine vaccine update, and yellow fever immunization. Factors independently associated with low compliance with antimalarials were traveling to the Indian Ocean or Asia, age <5 years, and monoparental family.
The authors want to thank Mrs Penny Hands for her kind help in the drafting of the manuscript.
The authors state they have no conflicts of interest to declare relevant to this article.