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Malaria risk perception, knowledge and prophylaxis practices among travellers of African ethnicity living in Paris and visiting their country of origin in sub-Saharan Africa
Transactions of the Royal Society of Tropical Medicine and Hygiene (2007) 101, 990—995
available at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/trst
Malaria risk perception, knowledge and prophylaxis practices among travellers of African ethnicity living in Paris and visiting their country of origin in sub-Saharan Africa T. Pistone a,b,c,d,∗, P. Guibert c, F. Gay c, D. Malvy c,d, K. Ezzedine d, e a,b, O. Bouchaud c,e M.C. Receveur c,d, M. Siriwardana a,b, B. Larouz´ a
INSERM, U707, Paris, F-75012, France Universit´ e Pierre et Marie Curie-Paris 6, UMR-S 707, Paris, F-75012, France c Soci´ et´ e de M´ edecine des Voyages, Paris, F-75017, France d Centre Ren´ e Labusqui` ere, Branche M´ edecine Tropicale, EA 3677, Universit´ e Victor Segalen Bordeaux 2, F-33076, France e Institut de M´ edecine et d’Epid´ emiologie Appliqu´ ees, Fondation Internationale L´ eon MBA, Hˆ opital Avicenne, Universit´ e Paris Nord, F-75018, France b
Received 6 August 2006; received in revised form 22 May 2007; accepted 22 May 2007 Available online 23 July 2007
KEYWORDS Malaria; Travel; Prophylaxis; Prevention; Migrants; Africa
Summary An observational prospective cohort study assessed malaria risk perception, knowledge and prophylaxis practices among individuals of African ethnicity living in Paris and travelling to their country of origin to visit friends or relatives (VFR). The study compared two groups of VFR who had visited a travel clinic (TC; n = 122) or a travel agency (TA; n = 69) before departure. Of the 47% of VFR citing malaria as a health concern, 75% knew that malaria is mosquito-borne and that bed nets are an effective preventive measure. Perception of high malaria risk was greater in the TA group (33%) than in the TC group (7%). The availability of a malaria vaccine was mentioned by 35% of VFR, with frequent confusion between yellow fever vaccine and malaria prevention. Twenty-nine percent took adequate chemoprophylaxis with complete adherence, which was higher among the TC group (41%) than the TA group (12%). Effective antivector protection measures used were bed nets (16%), wearing long clothes at night (14%) and air conditioning (8%), with no differences between the study groups except in the use of impregnated bed nets (11% of the TC group and none of the TA group). Media coverage, malaria chemoprophylaxis repayment and cultural adaptation of preventive messages should be improved to reduce the high rate of inadequate malaria prophylaxis in VFR. © 2007 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
∗ Corresponding author. Present address: Service de M´ edecine Interne et des Maladies Tropicales, Hˆ opital Sant-Andr´ e, CHU Bordeaux, France. Fax: +33 5 56 79 47 86. E-mail address: [email protected] (T. Pistone).
0035-9203/$ — see front matter © 2007 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2007.05.009
Malaria prophylaxis among travellers of African ethnicity
1. Introduction Among Western countries, France has the highest incidence of imported malaria cases owing to its historical links with French-speaking parts of Africa. The steady rise in imported malaria in France since the 1990s, acquired primarily in Africa, results in 6000—7000 cases and at least 20 avoidable deaths per year (Boutin et al., 2005). Imported malaria costs the French Public Health Insurance System around D 25 million annually (Pistone et al., 2003). Immigrants comprise less than 10% of France’s population but contribute more than 70% of imported malaria cases in the country (Boutin et al., 2005; Institut National de Statistiques et d’Economie, 2005). Previous studies have shown that the residents of Western countries most strongly affected by imported malaria are travellers of African ethnicity travelling to their country of origin to visit friends or relatives (VFR) (Boutin et al., 2005; Castelli et al., 1999; Cleary et al., 2003; Schultz, 1989; Shah et al., 1998). Thus, VFR are considered a high-risk group for imported malaria, and malaria prevention among these travellers should be improved by disseminating better information about malaria risk perception, knowledge and prophylaxis. Previous studies on VFR may suffer from recruitment bias because they focused on patients with a malaria attack. This problem appears to have been avoided in two recent investigations: one of African migrants attending a public health clinic in Italy (Scolari et al., 2002); and one of migrants living in London (Morgan and Figueroa-Munoz, 2005). However, neither study investigated VFR shortly before departure and immediately after return, the times when the most accurate data on prophylaxis knowledge and practice can be obtained. Therefore, we assessed malaria risk perception, knowledge and prophylaxis practices in pre-departure VFR at two travel agencies and two travel clinics in Paris. We also evaluated prophylactic practices in VFR upon return from their country of origin in sub-Saharan Africa.
2. Population and methods This observational prospective survey was conducted in Paris over an 8-month period (January—August 1998), evaluating VFR who visited their country of origin in sub-Saharan Africa for more than 7 days. Travellers were recruited on a volunteer basis by an investigator at two travel clinics (within Piti´ e-Salpˆ etri` ere and Bichat University Hospitals, Paris) after a pre-travel consultation (TC group) and in two travel agencies specialising in flights to sub-Saharan Africa after ticket purchase (TA group). Travellers recruited at both sites (TC and TA groups) and travellers of the TA group who intended to visit a travel clinic were not included in the study. The study had a pre-travel and post-travel phase and was based on interviews using a standardised questionnaire with open- and closed-ended questions. The pre-travel interviews, carried out face-to-face by the same investigator, provided information on social and demographic characteristics, knowledge and risk perception of malaria and planned prophylaxis practices. The study population was divided into eight socioeconomic levels according to the Public Institute of French Demography
991 (INSEE) and re-coded into three social classes: low (working class, unskilled employees), medium (skilled employees, technicians) or high (engineers, senior executives, company managers). Frequency of previous travel to Africa was classified into four groups: high (every 1—3 years), intermediate (every 4—7 years), low (every 8 years or more), or never since first arrival in France. In the post-travel phase, the same investigator interviewed by phone the travellers at most 10 days after their presumed date of return to Paris using a second standardised questionnaire concerning malaria prophylaxis practices, including chemoprophylaxis and antivector measures. Reproducibility of pre- and post-travel questionnaires was tested by phone. Both questionnaires were prospectively given twice within a 7-day interval among a randomised subset (15%) of the two groups and compared to assess validity. Answers to open-ended questions were analysed by identifying main themes and their frequency of appearance in the interviews. Malaria chemoprophylaxis adherence scores were calculated according to WHO specifications (WHO, 2005) as follows: percentage of days of malaria chemoprophylaxis adherence during travel and 30 days after. Chemoprophylaxis was considered ‘adequate’ for a given destination if the choice of drug, dosage and adherence were in accordance with the French national guidelines established by the Ministry of Health in 1998 (Conseil Sup´ erieur d’Hygi` ene Publique de France, 1998). Data entry, data management and univariate analysis were carried out using Epi Info 6.04 software (CDC, Atlanta, GA, USA). Differences were considered significant if the Pvalue was <0.05.
3. Results 3.1. Study population One hundred and ninety-one VFR were recruited and interviewed before their trip, 122 (64%) in the TC group and 69 (36%) in the TA group. For both groups, the median delay between interview and departure was 7 days. Forty-four travellers returned after the survey deadline (10 August 1998) and were not considered in the analysis. Of the 147 remaining, it was possible to contact 106 (72%; 64 TC group and 42 TA group) for phone interviews following their return to France. These individuals comprised the study population for the post-travel phase. The pre- and post-travel groups did not differ significantly in terms of gender, age, nationality, travel frequency, professional class or social and demographic characteristics (data available on request). Table 1 summarises the social and demographic characteristics of the TC and TA pre-travel groups of VFR. VFR from the TC group had a lower social level, a longer stay in France and had travelled less frequently to Africa. Travel destinations were linked to the country of origin. The most visited countries were Mali, Senegal, Ivory Coast and Cameroon for the TC group and Ivory Coast, Democratic Republic of Congo, Mali and Congo for the TA group. Ten percent (19/191) of all VFR visited Africa for the funeral ceremony of a relative.
992 Table 1
T. Pistone et al. Characteristics of the travel clinic (TC) and travel agency (TA) pre-travel groups of travellers of African ethnicity Total (N = 191) n (%)
TC group (N = 122) n (%)
TA group (N = 69) n (%)
P-value
37.8 111 (58) 180 (94) 51 (27) 162 (85)
37.9 72 (59) 112 (92) 36 (30) 104 (85)
37.70 39 (57) 68 (99) 15 (22) 58 (84)
0.91 0.74 0.11 0.34 0.99
Social class High Medium Low
23 (12) 81 (42) 87 (46)
13 (11) 42 (34) 67 (55)
10 (14) 39 (57) 20 (29)
0.002
Mean length of stay in France (years)
15.7
16.7
14.1
0.03
Frequency of previous travel to Africa Once every 1—3 years Once every 4—7 years Last trip ≥8 years ago Never
84 (44) 33 (17) 31 (16) 43 (23)
41 (34) 24 (20) 25 (20) 32 (26)
43 (62) 9 (13) 6 (9) 11 (16)
Median length of visit (days)
33
44
25
92 (75) 28 (23) 2 (2)
40 (58) 26 (38) 3 (4)
Mean age (years) Male African-born French citizenship Travel for family visit
Location of country visited West Africa Central Africa Indian Ocean
0.001
0.001 0.04
132 (69) 54 (28) 5 (3)
In the pre-travel population, 25% (48/191) of the VFR declared a history of a malaria attack.
3.2. Malaria risk perception and knowledge in the pre-travel population 3.2.1. Malaria risk perception and knowledge of malaria causes Of the 191 VFR in the pre-travel population, 49% (94/191) considered themselves at risk for contracting malaria, including 17% (32/191) who considered themselves at high risk. Perception of high malaria risk was greater (P < 0.05) in the TA group (33%; 23/69) than in the TC group (7%; 9/122). Answers to open-ended and closed-ended questions were mostly not statistically different between the TC and TA pretravel groups. Therefore, both groups were combined for the analyses (Tables 2 and 3). Concerning health risk perceptions and knowledge of malaria transmission (Table 2), malaria was mentioned by almost 50% of VFR in both groups and was by far the most frequent health concern. When VFR were asked how malaria is transmitted, 26% failed to mention mosquito bites, instead providing incorrect responses such as water transmission, poor personal hygiene and sun exposure. As shown in Table 3, which summarises general knowledge on malaria, 13% of VFR did not know they could catch malaria in the country they were visiting. Regarding prevention, 35% of the VFR were aware of the availability of a malaria vaccine and nearly two-thirds of the VFR considered that ‘they have to be vaccinated against malaria before travelling’—–highlighting the frequent confusion between yellow fever vaccination and malaria prevention.
Table 2 Analysis of main themes evoked in answers by travellers of African ethnicity to open-ended questions regarding health risk perceptions and knowledge of malaria transmissiona Analysis of main themes
Pre-travel populationb n (%)
‘What are your health concerns?’ (N = 191) Malaria Food- and water-borne diseases None AIDS Meningitis
89 (47) 49 (26) 45 (24) 13 (7) 10 (5)
‘For you, why is malaria a health concern?’ (N = 89) Inevitable destiny 60 (67) Mosquito bites impossible to prevent 22 (25) ‘For you, why is malaria not a health concern?’ (N = 102) Availability of chemoprophylaxis 45 (44) Availability of a vaccine 22 (22) Never had malaria attack 25 (25) ‘For you, how is malaria transmitted?’ (N = 191) Mosquito bites 141 (74) Water or poor personal hygiene 12 (6) Sun exposure 7 (4) a
No statistically significant differences between the travel clinic and travel agency groups. b More than one answer is possible to each question; therefore, total percentage for each question may be >100%.
Malaria prophylaxis among travellers of African ethnicity
993
Table 3 Analysis of answers by travellers of African ethnicity to five closed-ended questions regarding general malaria knowledgea General malaria knowledge
Yes n (%)
No n (%)
Do not know n (%)
‘Is it possible to get malaria in the country you are travelling to?’ ‘Is there a vaccine against malaria?’ ‘Does one have to be vaccinated against malaria before travelling?’ ‘Are skin repellents a good protection against malaria?’ ‘Is sleeping under a bed net a good protection against malaria?’
166 (87) 67 (35) 119 (62) 114 (60) 145 (76)
4 (2) 49 (26) 38 (20) 36 (19) 25 (13)
21 (11) 75 (39) 34 (18) 41 (21) 21 (11)
a
No statistically significant differences between the travel clinic and travel agency groups.
Fifty-two percent (99/191) believed that wearing long clothes at night is good protection against malaria, and this was higher in the TC group (58%; 71/122) than in the TA group (41%; 28/69) (P < 0.05). In response to the question ‘Do you have to take tablets against malaria up to 1 month after return to France?’, 65% (124/191) of VFR said ‘yes’, and this was higher in the TC group (72%; 88/122) than in the TA group (52%; 36/69) (P < 0.05). When asked ‘Do you know malaria prophylaxis measures?’, the VFR mentioned the key words ‘drugs’ (59%; 113/191), ‘Nivaquine® ’ (chloroquine) (31%; 59/191), ‘bed net’ (24%; 46/191) and ‘vaccination’ (16%; 30/191), with no differences between the TC and TA groups. 3.2.2. Prophylaxis planned before departure Ninety-four percent (179/191) of VFR planned to use a chemoprophylaxis, which was higher in the TC group (98%; 119/122) than in the TA group (87%; 60/69) (P < 0.05). In 59% (113/191) of the VFR (more frequently in the TC group (69%; 84/122) than in the TA group (42%; 29/69) (P < 0.05)) the intended regimen was adequate for the country they were visiting. In the pre-travel population, 51% (97/191) of TC and TA travellers intended to use at least one antivector measure (bed nets, long clothes or repellents). However, the planned use of bed nets was higher in the TC group (58%; 71/122) than in the TA group (32%; 22/69) (P < 0.05). Fifty-six percent (107/191) of VFR intended to use skin repellents and 10% (19/191) intended to use electric diffusers.
3.3. Malaria prophylaxis practices in the post-travel population As shown in Table 4, 75% (80/106) of the post-travel population said they had used a chemoprophylaxis (adequate
or not), including 15% who used chloroquine alone. Chemoprophylaxis use was more frequently reported in the TC group (86%; 55/64) than in the TA group (60%; 25/42) (P < 0.05). The median score of chemoprophylaxis adherence was higher in the TC group (93%; 51/55) than in the TA group (63%; 15/24) (P < 0.05). Fifty-seven percent (60/106) of VFR used a chemoprophylactic drug that was in accordance with the French national guidelines (Conseil Sup´ erieur d’Hygi` ene Publique de France, 1998). Adequate chemoprophylaxis practices (correct drug, dosage and adherence including after return) were reported by 29% (31/106) of the post-travel population, and this was higher in the TC group (41%; 26/64) than in the TA group (12%; 5/42) (P < 0.05). Our qualitative analysis of posttravel interviews identified three reasons for inadequate chemoprophylaxis after return: insufficient malaria risk perception; negligence; and absence of the drug after return to France, often because the drugs were left for relatives in Africa. Use of the following antivector protection measures was reported by the post-travel population: bed nets (16%; 17/106), long clothes in the evening (14%; 15/106), air conditioning (8%; 9/106), skin repellent (7%; 7/106) and mosquito coil (4%; 4/106). There was no significant difference between responses of the TC and TA groups, except for the use of impregnated bed nets (11% (7/64) of the TC group and none of the TA group).
4. Discussion Our findings highlight the paradoxical coupling of relatively good overall knowledge of malaria transmission and prophylaxis with a high rate of inadequate malaria prophylaxis in VFR. Numerous factors appeared to hinder the use of adequate protective measures, such as lower perceived risk of
Table 4 Chemoprophylaxis practices reported by the travel clinic (TC) and travel agency (TA) post-travel groups of travellers of African ethnicity Chemoprophylaxis practices (adequate or not) Chloroquine + proguanil Chloroquine alone Mefloquine Other None Total
Total (N = 106) n (%)
TC group (N = 64) n (%)
TA group (N = 42) n (%)
48 (45) 16 (15) 12 (11) 4 (4) 26 (25)
42 (66) 3 (5) 8 (13) 2 (3) 9 (14)
6 (14) 13 (31) 4 (10) 2 (5) 17 (40)
106 (100)
64 (100)
42 (100)
994 malaria attacks especially after return, absence of the drug after return to France, fatality and inadequate knowledge on transmission modes of malaria. These inadequate perceptions agree with the African social representation of malaria and have been reported in sub-Saharan Africa by several authors (Gessler et al., 1995; Morgan and Figueroa-Munoz, 2005; Nuwaha, 2002; Vundule and Mharakurwa, 1996). Moreover, incorrect belief that the yellow fever vaccine also works against malaria —– even after travel clinic advice — – may be an additional factor hindering the use of adequate protective measures in VFR. As suggested by Morgan and Figueroa-Munoz (2005), drug cost could also hamper adherence to prophylaxis. In this respect, Pistone et al. (2003) showed that reimbursing French travellers in West Africa for chloroquine plus proguanil malaria chemoprophylaxis could be cost effective for the French Public Health Insurance System. Further economic and sociological studies should be conducted to assess the impact of drug cost on recourse to chemoprophylaxis for VFR. As expected, the rate of adequate malaria chemoprophylaxis (29%) was higher in our study population of VFR than the rate of chemoprophylaxis (adequate or not) completed during the visit by imported malaria cases previously investigated (4—11%) (Bouchaud et al., 2005; Boutin et al., 2005; Castelli et al., 1999; Froude et al., 1992; Schultz, 1989; Shah et al., 1998). However, the rate observed among VFR was lower compared with rates (35—63%) observed among European travellers to malaria-endemic countries (Hamer and Connor, 2004; Laver et al., 2001; Malvy et al., 2006; Steffen et al., 1990). This result is consistent with the higher perception of malaria as a health risk among European travellers (Hamer and Connor, 2004; Toovey et al., 2004) compared with our study population (70% and 80% vs. 50%). We did not find significant differences between the TC and TA groups with regard to malaria risk perception and knowledge of the disease. Nevertheless, interpretation of these findings is limited by the relatively small number of VFR investigated. Furthermore, although we have carefully selected the population as described in Section 2, we cannot exclude the fact that a few subjects were misclassified. We identified several differences between VFR in the two groups. The TC group showed greater knowledge of prophylactic measures (pre-travel population) and higher rates of chemoprophylaxis use, including adequate regimens and better adherence (post-travel population). In addition, the differences between the two groups highlight greater knowledge among the TC group (pre-travel population) of two prophylactic measures —– duration of chemoprophylaxis after return to France and use of longsleeved clothing at night. These observations suggest the positive impact of pre-travel consultation in travel clinics regarding the implementation of adequate prophylactic measures. The drugs used by our study population for malaria prophylaxis emphasise the persistent common knowledge of chloroquine as a ‘well known’ chemoprophylactic drug even though its usage is no longer recommended as an efficient stand-alone drug for chemoprophylaxis in Africa. The widespread use of chloroquine as chemoprophylaxis and curative treatment for decades in Africa as well as its cheap price probably contribute to this persistent inadequate practice.
T. Pistone et al.
5. Conclusions Our findings regarding representations, somewhat limited knowledge on malaria and inadequate prophylactic practices identified in VRF demonstrate the need for public health strategies better adapted to this high-risk population. Culturally-targeted messages and media coverage must be developed, and chemoprophylaxis reimbursement needs to be considered by the French Public Health System. This should be done in collaboration with health workers in travel medicine, anthropologists and health education professionals. Authors’ contributions: PG and FG designed the study; PG carried out the data collection; TP, PG, FG, DM, BL and OB analysed the data; TP, PG, FG, DM, KE, MCR, BL, MS and OB interpreted the data. All authors were involved in the preparation of the manuscript and read and approved the final version. TP is guarantor of the paper. Acknowledgements: We thank Prof. Martin Danis, Dr Genevieve Brousse and Dr Catherine Voyer for accepting our investigation within the travel clinics of the Piti´ e-Salpˆ etri` ere and Bichat University Hospitals, Paris, France. We also thank Dr Paul Kretchmer (San Francisco Edit) for assistance in the revision of the English. Funding: None. Conflicts of interest: None declared. Ethical approval: Consultative Committee for Protection of Persons in Biological Research of the Piti´ e-Salpˆ etri` ere University Hospital, AP-HP, Paris, France.
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available at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/trst
Malaria risk perception, knowledge and prophylaxis practices among travellers of African ethnicity living in Paris and visiting their country of origin in sub-Saharan Africa T. Pistone a,b,c,d,∗, P. Guibert c, F. Gay c, D. Malvy c,d, K. Ezzedine d, e a,b, O. Bouchaud c,e M.C. Receveur c,d, M. Siriwardana a,b, B. Larouz´ a
INSERM, U707, Paris, F-75012, France Universit´ e Pierre et Marie Curie-Paris 6, UMR-S 707, Paris, F-75012, France c Soci´ et´ e de M´ edecine des Voyages, Paris, F-75017, France d Centre Ren´ e Labusqui` ere, Branche M´ edecine Tropicale, EA 3677, Universit´ e Victor Segalen Bordeaux 2, F-33076, France e Institut de M´ edecine et d’Epid´ emiologie Appliqu´ ees, Fondation Internationale L´ eon MBA, Hˆ opital Avicenne, Universit´ e Paris Nord, F-75018, France b
Received 6 August 2006; received in revised form 22 May 2007; accepted 22 May 2007 Available online 23 July 2007
KEYWORDS Malaria; Travel; Prophylaxis; Prevention; Migrants; Africa
Summary An observational prospective cohort study assessed malaria risk perception, knowledge and prophylaxis practices among individuals of African ethnicity living in Paris and travelling to their country of origin to visit friends or relatives (VFR). The study compared two groups of VFR who had visited a travel clinic (TC; n = 122) or a travel agency (TA; n = 69) before departure. Of the 47% of VFR citing malaria as a health concern, 75% knew that malaria is mosquito-borne and that bed nets are an effective preventive measure. Perception of high malaria risk was greater in the TA group (33%) than in the TC group (7%). The availability of a malaria vaccine was mentioned by 35% of VFR, with frequent confusion between yellow fever vaccine and malaria prevention. Twenty-nine percent took adequate chemoprophylaxis with complete adherence, which was higher among the TC group (41%) than the TA group (12%). Effective antivector protection measures used were bed nets (16%), wearing long clothes at night (14%) and air conditioning (8%), with no differences between the study groups except in the use of impregnated bed nets (11% of the TC group and none of the TA group). Media coverage, malaria chemoprophylaxis repayment and cultural adaptation of preventive messages should be improved to reduce the high rate of inadequate malaria prophylaxis in VFR. © 2007 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
∗ Corresponding author. Present address: Service de M´ edecine Interne et des Maladies Tropicales, Hˆ opital Sant-Andr´ e, CHU Bordeaux, France. Fax: +33 5 56 79 47 86. E-mail address: [email protected] (T. Pistone).
0035-9203/$ — see front matter © 2007 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.trstmh.2007.05.009
Malaria prophylaxis among travellers of African ethnicity
1. Introduction Among Western countries, France has the highest incidence of imported malaria cases owing to its historical links with French-speaking parts of Africa. The steady rise in imported malaria in France since the 1990s, acquired primarily in Africa, results in 6000—7000 cases and at least 20 avoidable deaths per year (Boutin et al., 2005). Imported malaria costs the French Public Health Insurance System around D 25 million annually (Pistone et al., 2003). Immigrants comprise less than 10% of France’s population but contribute more than 70% of imported malaria cases in the country (Boutin et al., 2005; Institut National de Statistiques et d’Economie, 2005). Previous studies have shown that the residents of Western countries most strongly affected by imported malaria are travellers of African ethnicity travelling to their country of origin to visit friends or relatives (VFR) (Boutin et al., 2005; Castelli et al., 1999; Cleary et al., 2003; Schultz, 1989; Shah et al., 1998). Thus, VFR are considered a high-risk group for imported malaria, and malaria prevention among these travellers should be improved by disseminating better information about malaria risk perception, knowledge and prophylaxis. Previous studies on VFR may suffer from recruitment bias because they focused on patients with a malaria attack. This problem appears to have been avoided in two recent investigations: one of African migrants attending a public health clinic in Italy (Scolari et al., 2002); and one of migrants living in London (Morgan and Figueroa-Munoz, 2005). However, neither study investigated VFR shortly before departure and immediately after return, the times when the most accurate data on prophylaxis knowledge and practice can be obtained. Therefore, we assessed malaria risk perception, knowledge and prophylaxis practices in pre-departure VFR at two travel agencies and two travel clinics in Paris. We also evaluated prophylactic practices in VFR upon return from their country of origin in sub-Saharan Africa.
2. Population and methods This observational prospective survey was conducted in Paris over an 8-month period (January—August 1998), evaluating VFR who visited their country of origin in sub-Saharan Africa for more than 7 days. Travellers were recruited on a volunteer basis by an investigator at two travel clinics (within Piti´ e-Salpˆ etri` ere and Bichat University Hospitals, Paris) after a pre-travel consultation (TC group) and in two travel agencies specialising in flights to sub-Saharan Africa after ticket purchase (TA group). Travellers recruited at both sites (TC and TA groups) and travellers of the TA group who intended to visit a travel clinic were not included in the study. The study had a pre-travel and post-travel phase and was based on interviews using a standardised questionnaire with open- and closed-ended questions. The pre-travel interviews, carried out face-to-face by the same investigator, provided information on social and demographic characteristics, knowledge and risk perception of malaria and planned prophylaxis practices. The study population was divided into eight socioeconomic levels according to the Public Institute of French Demography
991 (INSEE) and re-coded into three social classes: low (working class, unskilled employees), medium (skilled employees, technicians) or high (engineers, senior executives, company managers). Frequency of previous travel to Africa was classified into four groups: high (every 1—3 years), intermediate (every 4—7 years), low (every 8 years or more), or never since first arrival in France. In the post-travel phase, the same investigator interviewed by phone the travellers at most 10 days after their presumed date of return to Paris using a second standardised questionnaire concerning malaria prophylaxis practices, including chemoprophylaxis and antivector measures. Reproducibility of pre- and post-travel questionnaires was tested by phone. Both questionnaires were prospectively given twice within a 7-day interval among a randomised subset (15%) of the two groups and compared to assess validity. Answers to open-ended questions were analysed by identifying main themes and their frequency of appearance in the interviews. Malaria chemoprophylaxis adherence scores were calculated according to WHO specifications (WHO, 2005) as follows: percentage of days of malaria chemoprophylaxis adherence during travel and 30 days after. Chemoprophylaxis was considered ‘adequate’ for a given destination if the choice of drug, dosage and adherence were in accordance with the French national guidelines established by the Ministry of Health in 1998 (Conseil Sup´ erieur d’Hygi` ene Publique de France, 1998). Data entry, data management and univariate analysis were carried out using Epi Info 6.04 software (CDC, Atlanta, GA, USA). Differences were considered significant if the Pvalue was <0.05.
3. Results 3.1. Study population One hundred and ninety-one VFR were recruited and interviewed before their trip, 122 (64%) in the TC group and 69 (36%) in the TA group. For both groups, the median delay between interview and departure was 7 days. Forty-four travellers returned after the survey deadline (10 August 1998) and were not considered in the analysis. Of the 147 remaining, it was possible to contact 106 (72%; 64 TC group and 42 TA group) for phone interviews following their return to France. These individuals comprised the study population for the post-travel phase. The pre- and post-travel groups did not differ significantly in terms of gender, age, nationality, travel frequency, professional class or social and demographic characteristics (data available on request). Table 1 summarises the social and demographic characteristics of the TC and TA pre-travel groups of VFR. VFR from the TC group had a lower social level, a longer stay in France and had travelled less frequently to Africa. Travel destinations were linked to the country of origin. The most visited countries were Mali, Senegal, Ivory Coast and Cameroon for the TC group and Ivory Coast, Democratic Republic of Congo, Mali and Congo for the TA group. Ten percent (19/191) of all VFR visited Africa for the funeral ceremony of a relative.
992 Table 1
T. Pistone et al. Characteristics of the travel clinic (TC) and travel agency (TA) pre-travel groups of travellers of African ethnicity Total (N = 191) n (%)
TC group (N = 122) n (%)
TA group (N = 69) n (%)
P-value
37.8 111 (58) 180 (94) 51 (27) 162 (85)
37.9 72 (59) 112 (92) 36 (30) 104 (85)
37.70 39 (57) 68 (99) 15 (22) 58 (84)
0.91 0.74 0.11 0.34 0.99
Social class High Medium Low
23 (12) 81 (42) 87 (46)
13 (11) 42 (34) 67 (55)
10 (14) 39 (57) 20 (29)
0.002
Mean length of stay in France (years)
15.7
16.7
14.1
0.03
Frequency of previous travel to Africa Once every 1—3 years Once every 4—7 years Last trip ≥8 years ago Never
84 (44) 33 (17) 31 (16) 43 (23)
41 (34) 24 (20) 25 (20) 32 (26)
43 (62) 9 (13) 6 (9) 11 (16)
Median length of visit (days)
33
44
25
92 (75) 28 (23) 2 (2)
40 (58) 26 (38) 3 (4)
Mean age (years) Male African-born French citizenship Travel for family visit
Location of country visited West Africa Central Africa Indian Ocean
0.001
0.001 0.04
132 (69) 54 (28) 5 (3)
In the pre-travel population, 25% (48/191) of the VFR declared a history of a malaria attack.
3.2. Malaria risk perception and knowledge in the pre-travel population 3.2.1. Malaria risk perception and knowledge of malaria causes Of the 191 VFR in the pre-travel population, 49% (94/191) considered themselves at risk for contracting malaria, including 17% (32/191) who considered themselves at high risk. Perception of high malaria risk was greater (P < 0.05) in the TA group (33%; 23/69) than in the TC group (7%; 9/122). Answers to open-ended and closed-ended questions were mostly not statistically different between the TC and TA pretravel groups. Therefore, both groups were combined for the analyses (Tables 2 and 3). Concerning health risk perceptions and knowledge of malaria transmission (Table 2), malaria was mentioned by almost 50% of VFR in both groups and was by far the most frequent health concern. When VFR were asked how malaria is transmitted, 26% failed to mention mosquito bites, instead providing incorrect responses such as water transmission, poor personal hygiene and sun exposure. As shown in Table 3, which summarises general knowledge on malaria, 13% of VFR did not know they could catch malaria in the country they were visiting. Regarding prevention, 35% of the VFR were aware of the availability of a malaria vaccine and nearly two-thirds of the VFR considered that ‘they have to be vaccinated against malaria before travelling’—–highlighting the frequent confusion between yellow fever vaccination and malaria prevention.
Table 2 Analysis of main themes evoked in answers by travellers of African ethnicity to open-ended questions regarding health risk perceptions and knowledge of malaria transmissiona Analysis of main themes
Pre-travel populationb n (%)
‘What are your health concerns?’ (N = 191) Malaria Food- and water-borne diseases None AIDS Meningitis
89 (47) 49 (26) 45 (24) 13 (7) 10 (5)
‘For you, why is malaria a health concern?’ (N = 89) Inevitable destiny 60 (67) Mosquito bites impossible to prevent 22 (25) ‘For you, why is malaria not a health concern?’ (N = 102) Availability of chemoprophylaxis 45 (44) Availability of a vaccine 22 (22) Never had malaria attack 25 (25) ‘For you, how is malaria transmitted?’ (N = 191) Mosquito bites 141 (74) Water or poor personal hygiene 12 (6) Sun exposure 7 (4) a
No statistically significant differences between the travel clinic and travel agency groups. b More than one answer is possible to each question; therefore, total percentage for each question may be >100%.
Malaria prophylaxis among travellers of African ethnicity
993
Table 3 Analysis of answers by travellers of African ethnicity to five closed-ended questions regarding general malaria knowledgea General malaria knowledge
Yes n (%)
No n (%)
Do not know n (%)
‘Is it possible to get malaria in the country you are travelling to?’ ‘Is there a vaccine against malaria?’ ‘Does one have to be vaccinated against malaria before travelling?’ ‘Are skin repellents a good protection against malaria?’ ‘Is sleeping under a bed net a good protection against malaria?’
166 (87) 67 (35) 119 (62) 114 (60) 145 (76)
4 (2) 49 (26) 38 (20) 36 (19) 25 (13)
21 (11) 75 (39) 34 (18) 41 (21) 21 (11)
a
No statistically significant differences between the travel clinic and travel agency groups.
Fifty-two percent (99/191) believed that wearing long clothes at night is good protection against malaria, and this was higher in the TC group (58%; 71/122) than in the TA group (41%; 28/69) (P < 0.05). In response to the question ‘Do you have to take tablets against malaria up to 1 month after return to France?’, 65% (124/191) of VFR said ‘yes’, and this was higher in the TC group (72%; 88/122) than in the TA group (52%; 36/69) (P < 0.05). When asked ‘Do you know malaria prophylaxis measures?’, the VFR mentioned the key words ‘drugs’ (59%; 113/191), ‘Nivaquine® ’ (chloroquine) (31%; 59/191), ‘bed net’ (24%; 46/191) and ‘vaccination’ (16%; 30/191), with no differences between the TC and TA groups. 3.2.2. Prophylaxis planned before departure Ninety-four percent (179/191) of VFR planned to use a chemoprophylaxis, which was higher in the TC group (98%; 119/122) than in the TA group (87%; 60/69) (P < 0.05). In 59% (113/191) of the VFR (more frequently in the TC group (69%; 84/122) than in the TA group (42%; 29/69) (P < 0.05)) the intended regimen was adequate for the country they were visiting. In the pre-travel population, 51% (97/191) of TC and TA travellers intended to use at least one antivector measure (bed nets, long clothes or repellents). However, the planned use of bed nets was higher in the TC group (58%; 71/122) than in the TA group (32%; 22/69) (P < 0.05). Fifty-six percent (107/191) of VFR intended to use skin repellents and 10% (19/191) intended to use electric diffusers.
3.3. Malaria prophylaxis practices in the post-travel population As shown in Table 4, 75% (80/106) of the post-travel population said they had used a chemoprophylaxis (adequate
or not), including 15% who used chloroquine alone. Chemoprophylaxis use was more frequently reported in the TC group (86%; 55/64) than in the TA group (60%; 25/42) (P < 0.05). The median score of chemoprophylaxis adherence was higher in the TC group (93%; 51/55) than in the TA group (63%; 15/24) (P < 0.05). Fifty-seven percent (60/106) of VFR used a chemoprophylactic drug that was in accordance with the French national guidelines (Conseil Sup´ erieur d’Hygi` ene Publique de France, 1998). Adequate chemoprophylaxis practices (correct drug, dosage and adherence including after return) were reported by 29% (31/106) of the post-travel population, and this was higher in the TC group (41%; 26/64) than in the TA group (12%; 5/42) (P < 0.05). Our qualitative analysis of posttravel interviews identified three reasons for inadequate chemoprophylaxis after return: insufficient malaria risk perception; negligence; and absence of the drug after return to France, often because the drugs were left for relatives in Africa. Use of the following antivector protection measures was reported by the post-travel population: bed nets (16%; 17/106), long clothes in the evening (14%; 15/106), air conditioning (8%; 9/106), skin repellent (7%; 7/106) and mosquito coil (4%; 4/106). There was no significant difference between responses of the TC and TA groups, except for the use of impregnated bed nets (11% (7/64) of the TC group and none of the TA group).
4. Discussion Our findings highlight the paradoxical coupling of relatively good overall knowledge of malaria transmission and prophylaxis with a high rate of inadequate malaria prophylaxis in VFR. Numerous factors appeared to hinder the use of adequate protective measures, such as lower perceived risk of
Table 4 Chemoprophylaxis practices reported by the travel clinic (TC) and travel agency (TA) post-travel groups of travellers of African ethnicity Chemoprophylaxis practices (adequate or not) Chloroquine + proguanil Chloroquine alone Mefloquine Other None Total
Total (N = 106) n (%)
TC group (N = 64) n (%)
TA group (N = 42) n (%)
48 (45) 16 (15) 12 (11) 4 (4) 26 (25)
42 (66) 3 (5) 8 (13) 2 (3) 9 (14)
6 (14) 13 (31) 4 (10) 2 (5) 17 (40)
106 (100)
64 (100)
42 (100)
994 malaria attacks especially after return, absence of the drug after return to France, fatality and inadequate knowledge on transmission modes of malaria. These inadequate perceptions agree with the African social representation of malaria and have been reported in sub-Saharan Africa by several authors (Gessler et al., 1995; Morgan and Figueroa-Munoz, 2005; Nuwaha, 2002; Vundule and Mharakurwa, 1996). Moreover, incorrect belief that the yellow fever vaccine also works against malaria —– even after travel clinic advice — – may be an additional factor hindering the use of adequate protective measures in VFR. As suggested by Morgan and Figueroa-Munoz (2005), drug cost could also hamper adherence to prophylaxis. In this respect, Pistone et al. (2003) showed that reimbursing French travellers in West Africa for chloroquine plus proguanil malaria chemoprophylaxis could be cost effective for the French Public Health Insurance System. Further economic and sociological studies should be conducted to assess the impact of drug cost on recourse to chemoprophylaxis for VFR. As expected, the rate of adequate malaria chemoprophylaxis (29%) was higher in our study population of VFR than the rate of chemoprophylaxis (adequate or not) completed during the visit by imported malaria cases previously investigated (4—11%) (Bouchaud et al., 2005; Boutin et al., 2005; Castelli et al., 1999; Froude et al., 1992; Schultz, 1989; Shah et al., 1998). However, the rate observed among VFR was lower compared with rates (35—63%) observed among European travellers to malaria-endemic countries (Hamer and Connor, 2004; Laver et al., 2001; Malvy et al., 2006; Steffen et al., 1990). This result is consistent with the higher perception of malaria as a health risk among European travellers (Hamer and Connor, 2004; Toovey et al., 2004) compared with our study population (70% and 80% vs. 50%). We did not find significant differences between the TC and TA groups with regard to malaria risk perception and knowledge of the disease. Nevertheless, interpretation of these findings is limited by the relatively small number of VFR investigated. Furthermore, although we have carefully selected the population as described in Section 2, we cannot exclude the fact that a few subjects were misclassified. We identified several differences between VFR in the two groups. The TC group showed greater knowledge of prophylactic measures (pre-travel population) and higher rates of chemoprophylaxis use, including adequate regimens and better adherence (post-travel population). In addition, the differences between the two groups highlight greater knowledge among the TC group (pre-travel population) of two prophylactic measures —– duration of chemoprophylaxis after return to France and use of longsleeved clothing at night. These observations suggest the positive impact of pre-travel consultation in travel clinics regarding the implementation of adequate prophylactic measures. The drugs used by our study population for malaria prophylaxis emphasise the persistent common knowledge of chloroquine as a ‘well known’ chemoprophylactic drug even though its usage is no longer recommended as an efficient stand-alone drug for chemoprophylaxis in Africa. The widespread use of chloroquine as chemoprophylaxis and curative treatment for decades in Africa as well as its cheap price probably contribute to this persistent inadequate practice.
T. Pistone et al.
5. Conclusions Our findings regarding representations, somewhat limited knowledge on malaria and inadequate prophylactic practices identified in VRF demonstrate the need for public health strategies better adapted to this high-risk population. Culturally-targeted messages and media coverage must be developed, and chemoprophylaxis reimbursement needs to be considered by the French Public Health System. This should be done in collaboration with health workers in travel medicine, anthropologists and health education professionals. Authors’ contributions: PG and FG designed the study; PG carried out the data collection; TP, PG, FG, DM, BL and OB analysed the data; TP, PG, FG, DM, KE, MCR, BL, MS and OB interpreted the data. All authors were involved in the preparation of the manuscript and read and approved the final version. TP is guarantor of the paper. Acknowledgements: We thank Prof. Martin Danis, Dr Genevieve Brousse and Dr Catherine Voyer for accepting our investigation within the travel clinics of the Piti´ e-Salpˆ etri` ere and Bichat University Hospitals, Paris, France. We also thank Dr Paul Kretchmer (San Francisco Edit) for assistance in the revision of the English. Funding: None. Conflicts of interest: None declared. Ethical approval: Consultative Committee for Protection of Persons in Biological Research of the Piti´ e-Salpˆ etri` ere University Hospital, AP-HP, Paris, France.
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