Family Compliance With Counseling for Children Traveling to the Tropics
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1 171 ORIGINAL ARTICLE Family Compliance With Counseling for Children Traveling to the Tropics Stéphanie Caillet-Gossot, MD, Rémi Laporte, MD, Guilhem Noël, MD, Philippe Gautret, MD, PhD, Georges Soula, MD, Jean Delmont, MD, PhD, Benoit Faucher, MD, Philippe Parola, MD, PhD, Lindsay Osei, MD, and Philippe Minodier, MD Pediatric Emergency Unit; Center for Travel Medicine; Department of Infectious and Tropical Diseases, CHU Nord, Chemin des Bourrelly, Marseille, France DOI: /jtm Background. The number of people, both adults and children, traveling abroad, is on the rise. Some seek counseling at travel medicine centers before departure. Methods. A prospective study was conducted among children <16years visiting a travel medicine center in Marseille, France, from February 2010 to February Parents were contacted by telephone 4 weeks after their return, and asked about compliance with pre-travel advice. Results. 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. Conclusions. A 80% compliancewithpre-travel counselinginchildrentravelingoverseaswasachievedonly 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. 1 Their main purpose of travel is tourism, but some of them are visiting friends and relatives (VFR) abroad with their caregivers. 2 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. Materials and Methods The study took place in the Marseille Travel Medicine Center located in a tertiary university hospital in Corresponding Author: Philippe Minodier, MD, Pediatric Emergency Unit, Chemin des Bourrelly, F Marseille Cedex 20, France. philippe.minodier@ap-hm.fr southern France (CHU Nord, Marseille) from February 2010 to February 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, 5 which could introduce bias into the study. Pre-travel Visit Information on baseline demographics, type of journey, and children s previous vaccines was obtained. Children 2013 International Society of Travel Medicine, Journal of Travel Medicine 2013; Volume 20 (Issue 3):
2 172 Caillet-Gossot et al. Table 1 Demographics and travel features of children traveling to the tropics according to the purpose of the trip VFR children Tourist children Odds ratio n = 102 (%) n = 83 (%) [95% CI] p-value Age Mean (months, SD) 43 (43.0) 99 (50.0) < <5 years 72 (70.6) 18 (21.7) 8.7 [ ] < Family Mother born outside Europe 76 (74.5) 7 (5.4) 31.7 [ ] < State health insurance 38 (37.3 ) 3 (3.6) 15.8 [ ] < Monoparental family 28 (27.5) 9 (10.8) 3.1 [ ] children at home 45 (44.1) 20 (24.1) 2.5 [ ] Destination Africa 51 (50.0) 48 (57.8) 1 < Asia 1 (1.0) 17 (20.5) 0.06 [ ] Indian Ocean 43 (42.2) 5 (6.0) 8.09 [ ] South America 7 (6.9) 13 (15.7) 0.51 [ ] Local housing during travel (urban and/or rural housing) 102 (100.0) 53 (63.9) Not calculable < 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 [ ] < Mean time between pre-travel visit and departure (days, SD) 32 (23.0) 45 (30.0) < 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). 6 The discussion focused on travel-associated risks and their prevention. Routine vaccination updates and specific immunizations were recommended according to risk. 7 Depending on the risk of malaria and specific contraindications, chemoprophylaxis and protective measures against mosquitoes were prescribed 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. Telephone Questionnaire on Return 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 Collection and Statistical Analysis 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. Results Demographics and Travel Characteristics 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. Ninetynine (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
3 Compliance With Counseling in Traveling Children 173 Table 2 Prophylactic measures and compliance among children traveling to the tropics (N = 167 eligible children) Prophylactic measures Number of compliant children (%) 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 118/167 (70.7) vaccines 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 82/167 (52.7) salads Do not use ice cubes nor eat ice 121/167 (72.5) creams Do not buy food sold in the street 113/167 (67.7) Safe food and drinking water only 51/167 (30.5) VFR = visiting friends and relatives. Only children contacted by telephone after return are mentioned. 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). Compliance with Prophylactic Measures Table 2 reports the compliance with prophylactic measures among the 167 post-travel evaluated children. Immunizations Only 75 (41%) children were already fully immunized with routine vaccines. 7 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%). Malaria Chemoprophylaxis 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 < ). 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. Advice on Food and Water 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
4 174 Caillet-Gossot et al. Table 3 children) Factors associated with low compliance with atovaquone-proguanil or mefloquine chemoprophylaxis (N = 127 eligible Univariate Multivariate OR [95% CI] p aor [95% CI] p Age < 5 years 2.97 [ ] < [ ] 0.03 Monoparental family 3.22 [ ] < [ ] 0.04 Mother born outside Europe 2.02 [ ] [ ] 0.79 State health insurance 2.29 [ ] 0.12 VFR status 2.03 [ ] 0.12 Malaria chemoprophylaxis Atovaquone-proguanil Mefloquine 1.34 [ ] Destination Africa 1 < Asia 3.39 [ ] 6.73 [ ] Indian Ocean 5.76 [ ] 3.27 [ ] South America [0.0 ] aor = odds ratio adjusted by logistic regression, taking into account the effect of behavioral clustering in each family; VFR = visiting friends and relatives. All four children traveling to South America and receiving atovaquone-proguanil or mefloquine discontinued their treatment. with all recommended measures if the child was under 2 years in univariate analysis (OR = 4.38 [ ]). 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). Discussion 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. 11 The 66% malaria chemoprophylaxis compliance is consistent with other studies 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 19 (neither significant in this study). In fact, VFR people are an extremely varied group. 20 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. 21 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. 22 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. 23 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, 25 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,
5 Compliance With Counseling in Traveling Children 175 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. 26 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. Conclusion 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 foodand 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. Acknowledgment The authors want to thank Mrs Penny Hands for her kind help in the drafting of the manuscript. Declaration of Interests The authors state they have no conflicts of interest to declare relevant to this article. References 1. Guerin N, Sorge F, Imbert P, et al. Vaccinations for traveler child. Arch Pediatr 2007; 4: Gushulak BD, MacPherson DW. Globalization of infectious diseases: the impact of migration. Clin Infect Dis 2004; 38: Centers for Disease Control and Prevention. CDC health information for international travel New York, NY: Oxford University Press, Sorge F, Imbert P, Moulin F, et al. Moskito bite protection in children. Recommendations of the Groupe de Pédiatrie Tropicale. Arch Pediatr 2009; 16: McCarthy AE. Advising travelers with specific needs. In: Center for Disease Control and Prevention, eds. Yellow Book, Chapter 8. New York, NY: Oxford University Press, Available at: yellowbook/2012/chapter-8-advisingtravelers-with-specific-needs/long-term-travelersand-expatriates.htm. (Accessed 2012 Oct 2). 6. Keystone JS. Advising travelers with specific needs. In: Center for Disease Control and Prevention, eds. Yellow Book, Chapter 8. New York, NY: Oxford University Press, Available at: cdc.gov/travel/yellowbook/2012/chapter-8-advisingtravelers-with-specific-needs/immigrants-returninghome-to-visit-friends-and-relatives-vfrs.htm. (Accessed 2012 Oct 2). 7. Haut Conseil de la Santé Publique vaccination schedule and recommendations from the Haut Conseil de la Santé Publique. Bull Epidemiol Hebd 2009; 16 17: Haut Conseil de la Santé Publique. Health recommendations for travellers, Bull Epidemiol Hebd 2009; 18 19: Société de Pathologie Infectieuse de Langue Française, Collège des Universitaires de Maladies Infectieuses et Tropicales, Société Française de Médecine des Armées, et al. Management and prevention of imported Plasmodium falciparum malaria (Revision 2007 of the 1999 Consensus Conference). Med Mal Infect 2008; 38: PPAV Working Groups. Personal protection against biting insects and ticks. Parasite 2011; 18: Muller JM, Simonet AL, Binois R, et al. The respect of recommendations provided in an international travelers medical service: far from the cup to the lips. J Travel Med 2013; 20: Newman-Klee C, D Acremont V, Newman CJ, Gehri M, Genton B. Incidence and types of illness when traveling to the tropics: a prospective controlled study of children and their parents. Am J Trop Med Hyg 2007; 77: Hill D. Health problems in a large cohort of Americans traveling to developing countries. J Travel Med 2000; 7: Winer L, Alkan M. Incidence and precipitating factors of morbidity among Israeli travelers abroad. J Travel Med 2002; 9: Wilder-Smith A, Khairullah NS, Song JH, Chen CY, Torresi J. Travel health knowledge, attitudes and practices among Australasian travelers. J Travel Med 2004; 11: Van Herck K, Van Damme P, Castelli F, et al. Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey. J Travel Med 2004; 11: Arnaez J, Roa M, Albert L, et al. Imported malaria in children: a comparative study between recent immigrants and immigrant travelers (VFRs). J Travel Med 2010; 17: Leder K, Tong S, Weld L, et al. Illness in travelers visiting friends and relatives: a review of the GeoSentinel surveillance network. Clin Infect Dis 2006; 43: Boggild AK, Parise ME, Lewis LS, Kain KC. Atovaquoneproguanil: report from the CDC expert meeting on malaria chemoprophylaxis (II). Am J Trop Med Hyg 2007; 76: Schilthuis HJ, Goossens I, Ligthelm RJ, et al. Factors determining use of pre-travel preventive health services by West African immigrants in The Netherlands. Trop Med Int Health 2007; 12: Institut national de la statistique et des études économiques. Immigrés et descendants d immigrés en
6 176 Caillet-Gossot et al. France Insee références Edition Available at: sommaire.asp?codesage=immfra12&nivgeo=0. (Accessed 2012 Oct 10). 22. Fanello S, Hassani A, Meunier B, Dagorne C, Parot E. Consultation in a baby clinic of the PMI (mother and infant welfare service): a survey in a French department. Sante Publique 2007; 19: Bouhamam N, Laporte R, Boutin A, et al. Relationship between precariousness, social coverage, and vaccine coverage: survey among children consulting in pediatric emergency departments in France. Arch Pediatr 2012; 19: Steffen R, Tornieporth N, Costa Clemens SA, et al. Epidemiology of travelers diarrhea: details of a global survey. J Travel Med 2004; 11: Pitzinger B, Steffen R, Tschopp A. Incidence and clinical features of traveler s diarrhea in infants and children. Pediatr Infect Dis J 1991; 10: Sorge F, Guérin N, Imbert P, et al. Limiting factors of child traveller vaccinations: hepatitis A example. Arch Pediatr 2009; 16:
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