Imported malaria in young adults of Barcelona predominantly affected immigrants over five years of age who travelled to Africa (most frequently EG) to visit friends and relatives, did not complete chemoprophylaxis, were infected with P. falciparum and were treated without need of hospitalization. Age 15-19 years and VFR were associated factors to resident immigrants compared to natives. This study also found a decline in imported malaria incidence in recent years, which was not statistically significant.
As described in adult populations of similar settings in Spain and other European countries [8, 10, 13, 15, 16, 22–25], the majority of children affected by imported malaria in this study were African immigrants or children of African immigrants who travelled to sub-Saharan Africa [9, 13, 26, 27]. A recent analysis from the GeoSentinel Surveillance Network found that 69% of children needed hospitalization. Plasmodium falciparum accounted for 78% of all malaria cases, 95% of which were acquired in sub-Saharan Africa . A high number of malaria cases were found in EG immigrants and their children, which has been analysed in previous studies performed in Barcelona and other Spanish cities [18, 25, 28]. This high number of cases among Guinean population and the existence of two Tropical Medicine Units in the city, could explain the low percent of hospitalizations in Barcelona.
Many immigrants that are established residents in Spain visit their home country  with their children, who have rarely or never been exposed to malaria and thus possess little or null natural semi-immunity. These travellers are not accustomed to seek pre-travel advice or take chemoprophylaxis, although they travel to rural areas for longer periods of time [4, 7, 19]. A big concern is what Hagmann et al described in a recent study; VFR children were less likely than adults to receive pre travel medical advice . Like the rest of the travellers, resident immigrants and children who travel should be educated about the various preventative measures, such as barriers, impregnated nets and chemoprophylaxis completion for travel to endemic regions. Innovative methods to improve access to pre-travel services for VFR should be implemented [13, 14].
The association between imported malaria and VFR in patients under 20 years old has been reported in various European cities and countries [13, 18, 30] and was thoroughly described in a recent study about childhood malaria in England and Ireland . The characteristics of imported malaria cases found in our study, such as VFR travel reason, P. falciparum infection, and incomplete chemoprophylaxis use, are similar to those described in other cosmopolitan cities of the world [3, 21, 22]. Plasmodium falciparum is the most frequently identified species in children [26, 30, 31] not only in Barcelona, but also in the rest of Spain [8, 11, 32–36], other European countries [13, 15, 17, 26] and in the USA [6, 37, 38].
The infrequent use of chemoprophylaxis is a concern on a global scale. Although anti-malarial drug resistances are emerging in endemic countries, chemoprophylaxis is still effective and selection of a good regimen, along with barrier and repellent precautions, is key to decreasing the risk of acquiring malaria . The rate of correct chemoprophylaxis completion among cases in this study population is similar to that found in previous studies, which ranges from 3-15% [19, 31, 38]. These results demonstrate the severity of this problem. However, further evaluation is needed as we do not know how many people in the same age group in the general population travelled and performed chemoprophylaxis correctly. One explanation about the low chemoprophylaxis completion could be the false cultural idea that people born in endemic regions and their families are protected against malaria , underestimating the importance of disease and its potential fatality. It is also important to note that 28.7% of the resident immigrants travelling for VFR who did not complete chemoprophylaxis had previously suffered from malaria. Nonetheless, it would be important in the future differentiate if the previous malaria episode was in all the patients life or as a VFR. However, this percent is similar to the 26% found in a study from England in 2007 , and exposes an important missed opportunity for patient education about disease prevention. For example, assuming 90% effectiveness and 90% adherence, 105 of the 129 cases of malaria in resident immigrants could have been avoided.
The increase in incidence from 1990 to 1999 can be attributed to the high in international travel to endemic regions and infrequent use of chemoprophylaxis. The later decrease in incidence between 2000 and 2008 could be due to decreased incidence in endemic countries by the use of artemisinins and mosquito control programmes. Better travel advice, higher quality of travel health information in hospitals and primary care facilities and the correct use of chemoprophylaxis could also had a role in the decrease of incidence. There are many other factors that could also affect the incidence calculations such as migration flow, the census development and case reporting. Nonetheless, according to the linear trend analysis, the decline over the entire study period was not significant. Malaria incidence among children had not been previously described but one study from The Netherlands reported decreasing incidence among adults . The incidence of two cases per 100,000 reported in this study is slightly inferior to that reported in 2007 in the UK (2.8/100,000 per year) and Ireland (4.6/100,000 per year) in children less than 16 years of age . This difference could be due the high amount of immigration from endemic countries to the UK in comparison to Catalonia or Spain. Although arguably low, this incidence is not satisfactory for a preventable disease.
Studies that have assessed imported malaria among children have showed the important aspects of the clinical epidemiological patterns in various non-endemic countries [19, 40]. One strength of this study is the large study population. It is the first population-based study performed in Spain and provides incidence evolution over the last 18 years. The limitations of the study are the lack of clinical data information, reasons for hospitalization, as well as data about parents' country of birth. Immunology studies and patterns of travel among immigrants and the time spent as residents of a non-endemic country would also help us associate the disease with a level of semi-immunity in the future [41, 42].
The fatality rate was similar to previous studies performed in industrialized cities, except in Italy, Japan, Great Britain and Sweden, in which no deaths were reported [12, 26]. The vulnerability of the patients must not be forgotten, even though the lethality rate represents only one death. This patient was the son of immigrant parents from an endemic region, less than five years of age, who had travelled for VFR to a region of sub-Saharan Africa. He had never had malaria and did not complete chemoprophylaxis. Diagnostic delays of malaria are associated with higher rates of hospitalization and mortality, thus malaria should be considered for any child with a history of recent travel to an endemic country. This is especially important because malaria symptoms are non-specific and a diagnostic delay can be fatal [12, 13, 43].
Challenges for health systems in developed countries in the control of imported malaria include the improvement of information dissemination of preventative measures, the correct use of chemoprophylaxis when necessary and rapid diagnosis of clinical cases [43–45]. To reduce the risk of a diagnostic delay, protocols for primary care, emergency care and paediatric facilities should specify malaria as a possibility for immigrant patients and those who travel to an endemic region. Primary care teams working in areas of high immigration should also implement community activities to improve information availability and awareness. Furthermore, to promote their use, chemoprophylaxis recommendations should be available in most languages. Medicine is a dynamic and bio-psycho-social science in which many groups are involved and it is, therefore, necessary to quickly adapt to the needs of the population at any moment.