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Descriptive analysis of malaria prophylaxis for travellers from Greece visiting malaria-endemic countries
Travel Medicine and Infectious Disease (2011) 9, 284e288
Available online at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/tmid
Descriptive analysis of malaria prophylaxis for travellers from Greece visiting malaria-endemic countries Androula Pavli a,b, Paraskevi Smeti a,b, Athina Spilioti a,b, Annita Vakali a,b, Panagiotis Katerelos b, Helena C. Maltezou b,* a
Travel Medicine Office, Hellenic Centre for Disease Control and Prevention, 3-5 Agrafon Street, Athens 15123, Greece Department for Interventions in Health Care Facilities, Hellenic Centre for Disease Control and Prevention, 3-5 Agrafon Street, Athens 15123, Greece
b
Received 23 March 2011; received in revised form 26 September 2011; accepted 28 September 2011
KEYWORDS Malaria; Prophylaxis; Prescription; Travellers; Malaria-endemic countries
Summary International travel is changing the epidemiology of imported malaria. Our aim was to study malaria prophylaxis administered to travellers from Greece. The study was conducted during 2008e2009. Data were collected using a standardized form. A total of 2337 travellers were studied; prophylaxis was recommended to 60.2% of them. Of the 2337 travellers, 32.6% travelled to sub-Saharan Africa, 25.5% to South America, 11.8% to Indian subcontinent, 11.7% to Middle East, and 4.4% to Southeast Asia; prophylaxis was recommended to 77.4%, 64%, 80.6%, 4.8% and 73.5% of them, respectively. According to the purpose of travel, prophylaxis was recommended to 85.4% of those travelling for work, 75.2% of those visiting friends and relatives, and 62% of those travelling for recreation. Prophylaxis advised was provided to 68.5%, 66.2%, 61.5%, and 18.9% to those staying at a residence of local people, camping, hotels, and cruise ships, respectively. Regarding long-term travellers, malaria prophylaxis was recommended to 42.6%. Recommendation of malaria prophylaxis was significantly statistically in association with destination countries, purpose of travel, type of residence in endemic areas There is a need to improve recommendations for malaria prophylaxis for travellers from Greece, and to increase awareness and education of professionals providing travel health services in Greece. ª 2011 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ30 210 5212 175; fax: þ30 210 8899 330. E-mail address: [email protected] (H.C. Maltezou). 1477-8939/$ - see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tmaid.2011.09.005
Malaria prophylaxis for travellers from Greece
Introduction Malaria remains largely beyond control in over 100 tropical and subtropical countries, with an estimated annual global burden of 350e500 million infections and approximately 1 million deaths, of which 90% occur in sub-Saharan Africa.1e4 International travel is growing rapidly worldwide. An estimated 1.6 billion international journeys are expected by 2020, with the highest increase noted in tropical and subtropical areas.5 The increasing international travel in association with the enormous influx of immigrants from malaria-endemic countries had a significant impact on imported malaria cases in developed countries.6e8 Approximately 30,000 malaria cases occur each year in European and North American travellers returning from malaria-endemic countries.9 The current study was conducted by the Hellenic Centre for Disease Control and Prevention (Athens, Greece) in order to identify patterns of prescription of malaria prophylaxis for travellers visiting malaria-endemic countries who are seeking pre-travel advice in Greece.
Methods In Greece pre-travel advice, vaccinations, and antimalarial drugs (i.e. mefloquine, chloroquine, and primaquine) are provided by the Health Departments of 57 Prefectures across the country. Atovaquone/proguanil is not available and chloroquine is available exclusively in health departments. Health professionals providing travel health services include physicians specialized in public health or primary care, nurses, and health visitors. Mefloquine and atovaquone/proguanil can be prescribed by physicians working in travel clinics in private, public, and university hospitals, which are very few in the country. Pre-travel consultation services, malaria prevention advice, and vaccinations are provided in accordance with the national, World Health Organization, and the Centers for Disease Control and Prevention guidelines. All international travellers who attended all 57 Prefectures for pre-travel advice from January 1, 2008 through December 31, 2009, were asked to participate in a questionnaire-based study. Consent was requested from all participants The following data were collected prospectively using one standardized form per traveller: age, sex, date of departure, country of destination, duration of stay, type and purpose of travel, visiting areas, type of accommodation, participation in outdoor activities, and recommendation of malaria prophylaxis. Urban accommodation was defined as cities with population of 5000 people or greater, whereas rural accommodation was defined as villages of up to 5000 population or staying in the countryside. Short-term travel was defined as a trip of less than 1 month duration, while long-term travel was defined as a trip of 6 months or more. An organized trip was defined as a guided, package trip, mainly to popular tourist destinations. Outdoor activities include adventure sport, backpacking, hiking, and remote expedition. Malaria-endemic destinations were defined according to altitude, seasonality, intra-country variations (urban, rural), accommodation, activities and purpose of travel.
285 Statistical analysis was performed using the STATA 8.0 statistical package. The multivariable logistic regression was applied in order to investigate the relation between malaria prophylaxis prescription and travellers’ characteristics. The findings of the technique were re-examined using x2 test. A statistically significant relation was regarded as reliable if it was traced by both multivariate and univariate technique. P-values of 0.05 or less were considered statistically significant.
Results During the study period, 2700 travellers to malaria-endemic countries attended the 57 Health Departments, which constitutes only 2% of all travellers to developing countries of Africa, Asia, Central, and South America according to the Greek National Statistics Service (EL-STAT).10 Approximately 50% of the travellers attended the 7 Health Departments in the greater area of Athens. Information about malaria prophylaxis was available for 2337 (86.5%) travellers, which consisted the study group. Of the 2337 travellers, 60.3% were males; regarding age, 5.6%, 36.5%, 30%, 21.6%, and 6.3% of the travellers studied were 0e17 years old, 18e34 years old, 35e49 years old, 50e64 years old, and over 65 years old, respectively. Malaria prophylaxis was prescribed for 1408 (60.2%) of the 2337 travellers. According to the destination, 773 (33%) of them travelled to sub-Saharan Africa, 587 (25.11%) to South America, 290 (12.4%) to the Middle East, 278 (11.89%) to the Indian subcontinent, 98 (4.19%) to Southeast Asia, and 85 (3.63%) to Central America. Malaria prophylaxis was recommended to 77.4%, 64.1%, 4.8%, 80.6%, 73.5% and 22.4% of them, respectively (Table 1). According to the type of malaria prophylaxis, mefloquine was recommended to 68%, 64%, 63%, 61%, 60%, and 36.8% of those travelling to Southeast Asia, the Middle East, the Indian subcontinent, South America, sub-Saharan Africa, and Central America, respectively. Chloroquine was recommended to 47.4%, 7%, 5.3%, 2.2%, and 2.1% of those travelling to Central America, Middle East, East Asia, Indian subcontinent, and South Africa, respectively. Only 15 (1.1%) of all travellers were prescribed doxycycline and mainly travellers to subSaharan Africa. Atovaquone/proguanil was recommended to the rest of the travellers. Table 2 shows patterns of recommendation of malaria prophylaxis per travel characteristics. According to the type of travel, 1291 (55.2%) of the study group travelled on an organized trip, 685 (29.3%) travelled on a non-organized trip, 8 (0.34%) on a cruise, and for 353 (15.1%) this information was not available; malaria prophylaxis was prescribed to 777 (60.2%), 441 (64.4%), 3 (37.5%) and 187 (53.0%) of them, respectively. According to the area of stay, 1191 (51%) travellers stayed in urban areas, 71 (3.0%) in rural areas, 898 (38.42%) in urban and rural areas, while this information was not available in 177 (7.6%) travellers. Malaria prophylaxis was prescribed to 629 (52.8%), 50 (70.4%), 655 (72.9%) and 74 (41.8%) travellers, respectively. Regarding duration of travel, prophylaxis was recommended to 66.2% of short-term travellers and 42.6% of long-term travellers (p-value: not significant; Table 3). Data in relation to stand-by emergency treatment were not available. Recommendation of malaria
286
A. Pavli et al.
Table 1
Malaria prophylaxis recommendation according to destination.
Destination
Yes
Total N Z 2337
No
N Z 1408
N Z 929
(%)
(%)
High malaria endemicity (undisputed indication of malaria prophylaxis) Sub-Saharan Africa 598 (77.4) 175
(22.6)
773
Variable malaria transmission (variable indication of malaria prophylaxis) North Africa 11 (30.6) 25 South Africa 48 (73.8) 17 Indian Subcontinent 224 (80.6) 54 Southeast Asia 72 (73.5) 26 Eastern Asia 19 (43.2) 25 Middle East 14 (4.8) 276 South America 376 (64.1) 211 Central America 19 (22.4) 66
(69.4) (26.2) (19.4) (26.5) (56.8) (95.2) (35.9) (77.6)
36 65 278 98 44 290 587 85
Malaria not endemic (no indication of malaria prophylaxis) Europe 21 (46.7) North America 6 (17.6) Australia
(53.3) (82.4) (100.0)
45a 34a 2a
a
24 28 2
These destinations are 2nd or 3rd travel destinations.
prophylaxis was statistically significant in association with the destination countries, purpose of travel, type of residence in endemic areas, and involvement in outdoor activities (p-value < 0.001). Mosquito bite prevention (e.g. DEET, and adequate clothing) was recommended to all travellers to malaria-endemic areas.
Discussion Prescription of malaria prophylaxis depends on a riskbenefit analysis, weighting the risk of the disease against the risk of possible side effects of the drug.11 There are only few evidence-based studies available regarding the Table 2
risk of infection in travellers,12e15 thus there is a large variation of prescribed drugs in practice.16 Destination is the main factor for assessing the risk of acquisition of malaria.17e19 Using the GeoSentinel surveillance network database and statistics from the World Travel Organization, the relative risks for acquiring malaria per region visited compared with Europe and North America were: sub-Saharan Africa: 208, Oceania: 77, South Asia: 54, Central America: 38, Southeast Asia: 11.5, and South America: 8.20 As expected, our results showed statistically significant association between destination and recommendation of malaria prophylaxis, however the percentage of travellers to high risk destination of sub-Saharan Africa to whom prophylaxis was prescribed was lower (77.4%) than
Recommendation of malaria prophylaxis according to purpose of travel, place of residence, and outdoor activities.
Purpose of travel*
Yes N Z 1408
No
Total
(%)
N Z 929
(%)
N Z 2337
904 17 363 85 6 33
62.1 16.0 69.4 75.2 8.5 48.5
552 89 160 28 65 35
37.9 84.0 30.6 24.8 91.5 51.5
1456 106 523 113 71 68
Place of residence* Hotel Local house Cruise ship Camping Other Unknown
1058 224 25 43 22 36
61.5 68.5 18.9 66.2 75.9 55.4
661 103 107 22 7 29
38.5 31.5 81.1 33.8 24.1 44.6
1719 327 132 65 29 65
Outdoor activities Yes No
184 1224
71.4 58.9
74 855
28.7 41.1
258 2079
Recreation Sailors Work Visiting friends and relatives Religious reasons Unknown
*p-value < 0.001.
Malaria prophylaxis for travellers from Greece
287
Table 3 Malaria prophylaxis recommendation according to duration of travel. Duration of travel <1 month 1e3 months 3e6 months 6 months Unknown
Yes
No
Total
NZ
(%)
NZ
(%)
N Z 2337
1103 174 46 46 39
66.2 44.8 42.2 42.6 59.1
563 214 63 62 27
33.8 55.2 57.8 57.4 40.9
1666 388 109 108 66
expected. Of note, the proportion of travellers to the Indian subcontinent for whom malaria prophylaxis was prescribed (80.6%) was higher than the proportion of travellers to sub-Saharan Africa for whom prophylaxis was prescribed, which suggests non-selective prescription patterns for travellers to this destination. Analysis of malaria imported into eight European countries from the Indian subcontinent, led to a consensus statement by the TropNetEurop group recommending that non-selective prescription of prophylaxis for visitors to India, Pakistan, Bangladesh, and Sri Lanka should be dropped.21 In our study 75% of travellers visiting friends and relatives (VFRs) were prescribed prophylaxis. Travellers VFRs have the highest risk for acquisition of malaria compared to non-VFRs,20,22e28 and data from GeoSentinel showed that migrants VFRs were 4.5 times more likely to acquire malaria compared with tourist travellers, and this increase was even greater (8-fold) when travel destination concerned sub-Saharan African countries.27 VFRs typically demonstrate travel and behavioural patterns which render them at high risk for malaria. Pre-travel services are rarely sought by VFRs, whereas misconception that they possess life-long immunity against malaria make them less likely to receive or adhere to malaria prophylaxis recommendations. In addition, VFRs may face difficulties in accessing healthcare services because of economic, cultural, language, or legal issues.20,22e28 Long-term travellers are at higher risk for malaria acquisition due to poor compliance to continuous malaria prophylaxis and personal protective measures,27,29e31 while malaria prophylaxis recommendations for long-term travellers have not been standardized.31 In our study, 42.6% of long-term travellers were prescribed prophylaxis. Outdoor activities and staying in camping, cheap accommodations, or rural homes also represent risks for acquisition of malaria,8,32 however malaria prophylaxis was prescribed only in two thirds of our travellers with these characteristics. Our results show that malaria prophylaxis recommendations for travellers from Greece travelling to malaria endemic countries are generally within expectations. However, considering the very low number of travellers seeking pretravel health advice, increasing awareness about malaria transmission is very important. Travel health consultants should be educated about risk factors for acquisition of malaria and schedule prevention strategies accordingly.
Conflict of interest None.
References 1. Reiter P. Global warming and malaria: knowing the horse before hitching the cart. Malar J 2008;7(Suppl 1):S3. 2. Sachs J, Pia M. The economic and social burden of malaria. Nature 2002;415:680e5. 3. Roll Back Malaria. Global malaria action Plan. available at: http://www.rollbackmalaria.org/keyfacts.html; 2008 [accessed 28.12.10]. 4. Malaria Ehrhardt S In: Maltezou HC, Gikas A, editors. Tropical and emerging infectious diseases. Kerala, India: Research Signpost; 2010. p. 147e62. 5. World Tourism Organization. Tourism 2020 vision, available at: www.world-tourism.org [accessed 28.12.10]. 6. Mali S, Steele S, Slutsker L, Arguin PM. Malaria surveillanceUnited States, 2006. MMWR Morb Mortal Wkly Rep 2008;(57): 24e39. 7. Romi R, Sabatinelli G, Majori G. Malaria epidemiological situation in Italy and evaluation of malaria incidence in Italian travellers. J Travel Med 2001;8:6e11. 8. Malaria. International travel and health, available at: http:// www.who.int/ith/ITH2010chapter7.pdf [accessed 28.12.10]. 9. Keystone JS, Steffen R, Kozarsky PE. Health advice for international traveller. In: Guerrant RL, Walker DH, Weller PF, editors. Tropical infectious diseases: principles, pathogens, and practice, vol. 2. Philadelphia: Churchill Livingstone Elsevier; 2006. p. 1400e24. 10. Hellenic statistical authority, available at: http://www. statistics.gr/portal/page/portal/ESYE/PAGE-database, [accessed 8.07.11]. 11. Schlagenhauf P, Petersen E. Malaria chemoprophylaxis: strategies for risk groups. Clin Microbiol Rev 2008;21:466e72. 12. Phillips-Howard PA, Radalowicz A, Mitchell J, Bradley DJ. Risk of malaria in British residents returning from malarious areas. BMJ 1990;300:499e503. 13. Steffen R, Fuchs E, Schildknecht J, Naef U, Funk M, Schlagenhauf P, et al. Mefloquine compared with other malaria chemoprophylactic regimens in tourists visiting East Africa. Lancet 1993;341:1299e303. 14. Overbosch D, Schilthuis H, Bienzle U, Behrens RH, Kain KC, Clarke PD, et al. Malarone international study team. Atovaquoneproguanil versus mefloquine for malaria prophylaxis in nonimmune travellers: results from a randomized, doubleblind study. Clin Infect Dis 2001;33:1015e21. 15. Schlagenhauf P, Tschopp A, Johnson R, Nothdurft HD, Beck B, Schwartz E, et al. Tolerability of malaria chemoprophylaxis in non-immune travellers to sub-Saharan Africa: multicentre, randomised randomised, double blind, four arm study. BMJ 2003;327:1078. 16. Calleri G, Behrens RH, Bisoffi Z, Bjorkman A, Castelli F, Gascon J, et al. Variability in malaria prophylaxis prescribing across Europe: a Delphi method analysis. J Travel Med 2008; 15:294e301. 17. Freedman DO, Weld LH, Kozarsky PE, Fisk T, Robins R, von Sonnenburg F, et al. Spectrum of disease and relation to place of exposure among ill returned travellers. N Engl J Med 2006; 354:119e30. 18. Gautret P, Schlagenhauf P, Gaudart J, Castelli F, Brouqui P, von Sonnenburg F, et al. Multicenter EuroTravNet/GeoSentinel study of travel-related infectious disease in Europe. Emerg Infect Dis 2009;15:1783e90. 19. Field V, Gautret P, Schlagenhauf P, Burchard GD, Caumes E, Jensenius M, et al. Travel and migration associated infectious diseases morbidity in Europe, 2008. BMC Infect Dis 2010;10: 330. 20. Fenner L, Weber R, Steffen R, Schlagenhauf P. Imported infectious disease and purpose of travel. Switzerland Emerg Infect Dis 2007;13:217e22.
288 21. Behrens RH, Bisoffi Z, Bjo ¨rkman A, Gascon J, Hatz C, Jelinek T, et al. Malaria prophylaxis policy for travellers from Europe to the Indian subcontinent. Malar J 2006;1:5e7. 22. Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, et al. Illness in travellers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 2006;43:1185e94. 23. Angell SY, Cetron MS. Health disparities among travellers visiting friends and relatives abroad. Ann Intern Med 2005;142:67e72. 24. Angell SY, Behrens RH. Risk assessment and disease prevention in travellers visiting friends and relatives. Infect Dis Clin N Am 2005;19:49e65. 25. Bacaner N, Stauffer B, Boulware DR, Walker PF, Keystone JS. Travel medicine considerations for North American immigrants visiting friends and relatives. JAMA 2004;291:2856e64. 26. Pavli A, Katerelos P, Pierroutsakos P, Maltezou HC. Pre-travel counselling in Greece for travellers visiting friends and relatives. Trav Med Infect Dis 2009;7:312e5.
A. Pavli et al. 27. Leder K, Black J, O’Brien D, Greenwood Z, Kain KC, Schwartz E, et al. Malaria in travellers: a review of the GeoSentinel surveillance network. Clin Infect Dis 2004;39:1104e39. 28. Barnett ED, MacPherson DW, Stauffer WM, Loutan L, Hatz CF, Matteelli A, et al. The visiting friends or relatives traveller in the 21st century: time for a new definition. J Travel Med 2010; 17:163e70. 29. Toovey S, Moerman F, van Gompel A. Special infectious disease risks of expatriates and long-term travellers in tropical countries. Part I: malaria. J Travel Med 2007 JanFeb;14:42e9. 30. Chen LH, Wilson ME, Davis X, Loutan L, Schwartz E, Keystone J, et al. Illness in long-term travellers visiting GeoSentinel clinics. Emerg Infect Dis 2009;15:1773e82. 31. Chen LH, Wilson ME, Schlagenhauf P. Prevention of malaria in long-term travellers. JAMA 2006 Nov 8;296:2234e44. 32. Leggat PA, Shaw MM. Travel health advice for backpackers. J Travel Med 2003;10:340e5.
Available online at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/tmid
Descriptive analysis of malaria prophylaxis for travellers from Greece visiting malaria-endemic countries Androula Pavli a,b, Paraskevi Smeti a,b, Athina Spilioti a,b, Annita Vakali a,b, Panagiotis Katerelos b, Helena C. Maltezou b,* a
Travel Medicine Office, Hellenic Centre for Disease Control and Prevention, 3-5 Agrafon Street, Athens 15123, Greece Department for Interventions in Health Care Facilities, Hellenic Centre for Disease Control and Prevention, 3-5 Agrafon Street, Athens 15123, Greece
b
Received 23 March 2011; received in revised form 26 September 2011; accepted 28 September 2011
KEYWORDS Malaria; Prophylaxis; Prescription; Travellers; Malaria-endemic countries
Summary International travel is changing the epidemiology of imported malaria. Our aim was to study malaria prophylaxis administered to travellers from Greece. The study was conducted during 2008e2009. Data were collected using a standardized form. A total of 2337 travellers were studied; prophylaxis was recommended to 60.2% of them. Of the 2337 travellers, 32.6% travelled to sub-Saharan Africa, 25.5% to South America, 11.8% to Indian subcontinent, 11.7% to Middle East, and 4.4% to Southeast Asia; prophylaxis was recommended to 77.4%, 64%, 80.6%, 4.8% and 73.5% of them, respectively. According to the purpose of travel, prophylaxis was recommended to 85.4% of those travelling for work, 75.2% of those visiting friends and relatives, and 62% of those travelling for recreation. Prophylaxis advised was provided to 68.5%, 66.2%, 61.5%, and 18.9% to those staying at a residence of local people, camping, hotels, and cruise ships, respectively. Regarding long-term travellers, malaria prophylaxis was recommended to 42.6%. Recommendation of malaria prophylaxis was significantly statistically in association with destination countries, purpose of travel, type of residence in endemic areas There is a need to improve recommendations for malaria prophylaxis for travellers from Greece, and to increase awareness and education of professionals providing travel health services in Greece. ª 2011 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ30 210 5212 175; fax: þ30 210 8899 330. E-mail address: [email protected] (H.C. Maltezou). 1477-8939/$ - see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tmaid.2011.09.005
Malaria prophylaxis for travellers from Greece
Introduction Malaria remains largely beyond control in over 100 tropical and subtropical countries, with an estimated annual global burden of 350e500 million infections and approximately 1 million deaths, of which 90% occur in sub-Saharan Africa.1e4 International travel is growing rapidly worldwide. An estimated 1.6 billion international journeys are expected by 2020, with the highest increase noted in tropical and subtropical areas.5 The increasing international travel in association with the enormous influx of immigrants from malaria-endemic countries had a significant impact on imported malaria cases in developed countries.6e8 Approximately 30,000 malaria cases occur each year in European and North American travellers returning from malaria-endemic countries.9 The current study was conducted by the Hellenic Centre for Disease Control and Prevention (Athens, Greece) in order to identify patterns of prescription of malaria prophylaxis for travellers visiting malaria-endemic countries who are seeking pre-travel advice in Greece.
Methods In Greece pre-travel advice, vaccinations, and antimalarial drugs (i.e. mefloquine, chloroquine, and primaquine) are provided by the Health Departments of 57 Prefectures across the country. Atovaquone/proguanil is not available and chloroquine is available exclusively in health departments. Health professionals providing travel health services include physicians specialized in public health or primary care, nurses, and health visitors. Mefloquine and atovaquone/proguanil can be prescribed by physicians working in travel clinics in private, public, and university hospitals, which are very few in the country. Pre-travel consultation services, malaria prevention advice, and vaccinations are provided in accordance with the national, World Health Organization, and the Centers for Disease Control and Prevention guidelines. All international travellers who attended all 57 Prefectures for pre-travel advice from January 1, 2008 through December 31, 2009, were asked to participate in a questionnaire-based study. Consent was requested from all participants The following data were collected prospectively using one standardized form per traveller: age, sex, date of departure, country of destination, duration of stay, type and purpose of travel, visiting areas, type of accommodation, participation in outdoor activities, and recommendation of malaria prophylaxis. Urban accommodation was defined as cities with population of 5000 people or greater, whereas rural accommodation was defined as villages of up to 5000 population or staying in the countryside. Short-term travel was defined as a trip of less than 1 month duration, while long-term travel was defined as a trip of 6 months or more. An organized trip was defined as a guided, package trip, mainly to popular tourist destinations. Outdoor activities include adventure sport, backpacking, hiking, and remote expedition. Malaria-endemic destinations were defined according to altitude, seasonality, intra-country variations (urban, rural), accommodation, activities and purpose of travel.
285 Statistical analysis was performed using the STATA 8.0 statistical package. The multivariable logistic regression was applied in order to investigate the relation between malaria prophylaxis prescription and travellers’ characteristics. The findings of the technique were re-examined using x2 test. A statistically significant relation was regarded as reliable if it was traced by both multivariate and univariate technique. P-values of 0.05 or less were considered statistically significant.
Results During the study period, 2700 travellers to malaria-endemic countries attended the 57 Health Departments, which constitutes only 2% of all travellers to developing countries of Africa, Asia, Central, and South America according to the Greek National Statistics Service (EL-STAT).10 Approximately 50% of the travellers attended the 7 Health Departments in the greater area of Athens. Information about malaria prophylaxis was available for 2337 (86.5%) travellers, which consisted the study group. Of the 2337 travellers, 60.3% were males; regarding age, 5.6%, 36.5%, 30%, 21.6%, and 6.3% of the travellers studied were 0e17 years old, 18e34 years old, 35e49 years old, 50e64 years old, and over 65 years old, respectively. Malaria prophylaxis was prescribed for 1408 (60.2%) of the 2337 travellers. According to the destination, 773 (33%) of them travelled to sub-Saharan Africa, 587 (25.11%) to South America, 290 (12.4%) to the Middle East, 278 (11.89%) to the Indian subcontinent, 98 (4.19%) to Southeast Asia, and 85 (3.63%) to Central America. Malaria prophylaxis was recommended to 77.4%, 64.1%, 4.8%, 80.6%, 73.5% and 22.4% of them, respectively (Table 1). According to the type of malaria prophylaxis, mefloquine was recommended to 68%, 64%, 63%, 61%, 60%, and 36.8% of those travelling to Southeast Asia, the Middle East, the Indian subcontinent, South America, sub-Saharan Africa, and Central America, respectively. Chloroquine was recommended to 47.4%, 7%, 5.3%, 2.2%, and 2.1% of those travelling to Central America, Middle East, East Asia, Indian subcontinent, and South Africa, respectively. Only 15 (1.1%) of all travellers were prescribed doxycycline and mainly travellers to subSaharan Africa. Atovaquone/proguanil was recommended to the rest of the travellers. Table 2 shows patterns of recommendation of malaria prophylaxis per travel characteristics. According to the type of travel, 1291 (55.2%) of the study group travelled on an organized trip, 685 (29.3%) travelled on a non-organized trip, 8 (0.34%) on a cruise, and for 353 (15.1%) this information was not available; malaria prophylaxis was prescribed to 777 (60.2%), 441 (64.4%), 3 (37.5%) and 187 (53.0%) of them, respectively. According to the area of stay, 1191 (51%) travellers stayed in urban areas, 71 (3.0%) in rural areas, 898 (38.42%) in urban and rural areas, while this information was not available in 177 (7.6%) travellers. Malaria prophylaxis was prescribed to 629 (52.8%), 50 (70.4%), 655 (72.9%) and 74 (41.8%) travellers, respectively. Regarding duration of travel, prophylaxis was recommended to 66.2% of short-term travellers and 42.6% of long-term travellers (p-value: not significant; Table 3). Data in relation to stand-by emergency treatment were not available. Recommendation of malaria
286
A. Pavli et al.
Table 1
Malaria prophylaxis recommendation according to destination.
Destination
Yes
Total N Z 2337
No
N Z 1408
N Z 929
(%)
(%)
High malaria endemicity (undisputed indication of malaria prophylaxis) Sub-Saharan Africa 598 (77.4) 175
(22.6)
773
Variable malaria transmission (variable indication of malaria prophylaxis) North Africa 11 (30.6) 25 South Africa 48 (73.8) 17 Indian Subcontinent 224 (80.6) 54 Southeast Asia 72 (73.5) 26 Eastern Asia 19 (43.2) 25 Middle East 14 (4.8) 276 South America 376 (64.1) 211 Central America 19 (22.4) 66
(69.4) (26.2) (19.4) (26.5) (56.8) (95.2) (35.9) (77.6)
36 65 278 98 44 290 587 85
Malaria not endemic (no indication of malaria prophylaxis) Europe 21 (46.7) North America 6 (17.6) Australia
(53.3) (82.4) (100.0)
45a 34a 2a
a
24 28 2
These destinations are 2nd or 3rd travel destinations.
prophylaxis was statistically significant in association with the destination countries, purpose of travel, type of residence in endemic areas, and involvement in outdoor activities (p-value < 0.001). Mosquito bite prevention (e.g. DEET, and adequate clothing) was recommended to all travellers to malaria-endemic areas.
Discussion Prescription of malaria prophylaxis depends on a riskbenefit analysis, weighting the risk of the disease against the risk of possible side effects of the drug.11 There are only few evidence-based studies available regarding the Table 2
risk of infection in travellers,12e15 thus there is a large variation of prescribed drugs in practice.16 Destination is the main factor for assessing the risk of acquisition of malaria.17e19 Using the GeoSentinel surveillance network database and statistics from the World Travel Organization, the relative risks for acquiring malaria per region visited compared with Europe and North America were: sub-Saharan Africa: 208, Oceania: 77, South Asia: 54, Central America: 38, Southeast Asia: 11.5, and South America: 8.20 As expected, our results showed statistically significant association between destination and recommendation of malaria prophylaxis, however the percentage of travellers to high risk destination of sub-Saharan Africa to whom prophylaxis was prescribed was lower (77.4%) than
Recommendation of malaria prophylaxis according to purpose of travel, place of residence, and outdoor activities.
Purpose of travel*
Yes N Z 1408
No
Total
(%)
N Z 929
(%)
N Z 2337
904 17 363 85 6 33
62.1 16.0 69.4 75.2 8.5 48.5
552 89 160 28 65 35
37.9 84.0 30.6 24.8 91.5 51.5
1456 106 523 113 71 68
Place of residence* Hotel Local house Cruise ship Camping Other Unknown
1058 224 25 43 22 36
61.5 68.5 18.9 66.2 75.9 55.4
661 103 107 22 7 29
38.5 31.5 81.1 33.8 24.1 44.6
1719 327 132 65 29 65
Outdoor activities Yes No
184 1224
71.4 58.9
74 855
28.7 41.1
258 2079
Recreation Sailors Work Visiting friends and relatives Religious reasons Unknown
*p-value < 0.001.
Malaria prophylaxis for travellers from Greece
287
Table 3 Malaria prophylaxis recommendation according to duration of travel. Duration of travel <1 month 1e3 months 3e6 months 6 months Unknown
Yes
No
Total
NZ
(%)
NZ
(%)
N Z 2337
1103 174 46 46 39
66.2 44.8 42.2 42.6 59.1
563 214 63 62 27
33.8 55.2 57.8 57.4 40.9
1666 388 109 108 66
expected. Of note, the proportion of travellers to the Indian subcontinent for whom malaria prophylaxis was prescribed (80.6%) was higher than the proportion of travellers to sub-Saharan Africa for whom prophylaxis was prescribed, which suggests non-selective prescription patterns for travellers to this destination. Analysis of malaria imported into eight European countries from the Indian subcontinent, led to a consensus statement by the TropNetEurop group recommending that non-selective prescription of prophylaxis for visitors to India, Pakistan, Bangladesh, and Sri Lanka should be dropped.21 In our study 75% of travellers visiting friends and relatives (VFRs) were prescribed prophylaxis. Travellers VFRs have the highest risk for acquisition of malaria compared to non-VFRs,20,22e28 and data from GeoSentinel showed that migrants VFRs were 4.5 times more likely to acquire malaria compared with tourist travellers, and this increase was even greater (8-fold) when travel destination concerned sub-Saharan African countries.27 VFRs typically demonstrate travel and behavioural patterns which render them at high risk for malaria. Pre-travel services are rarely sought by VFRs, whereas misconception that they possess life-long immunity against malaria make them less likely to receive or adhere to malaria prophylaxis recommendations. In addition, VFRs may face difficulties in accessing healthcare services because of economic, cultural, language, or legal issues.20,22e28 Long-term travellers are at higher risk for malaria acquisition due to poor compliance to continuous malaria prophylaxis and personal protective measures,27,29e31 while malaria prophylaxis recommendations for long-term travellers have not been standardized.31 In our study, 42.6% of long-term travellers were prescribed prophylaxis. Outdoor activities and staying in camping, cheap accommodations, or rural homes also represent risks for acquisition of malaria,8,32 however malaria prophylaxis was prescribed only in two thirds of our travellers with these characteristics. Our results show that malaria prophylaxis recommendations for travellers from Greece travelling to malaria endemic countries are generally within expectations. However, considering the very low number of travellers seeking pretravel health advice, increasing awareness about malaria transmission is very important. Travel health consultants should be educated about risk factors for acquisition of malaria and schedule prevention strategies accordingly.
Conflict of interest None.
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