Imported malaria cases: the connection with the European ex-colonies

The epidemiological profile of malaria cases in this series is: young individual between 15 and 39 years old, VFR, from sub-Saharan Africa (particularly from Equatorial Guinea), and resident in the main province which is mostly urban. This patient profile coincides with that observed in other studies [7, 18‐20], included that published recently [16].

The increase on the imported malaria cases in non-endemic areas like Spain has been described [1, 16], but since these reports end in 2015, they do not show the pronounced more recent increase, with a peak in 2017. The reason for this increment is unclear; it could be due to social changes that involve making more trips to tropical areas, perhaps there is less and less awareness of prevention. What is clear is that it is necessary to stop this increase.

Aragonese cases are distributed in a greater percentage (45.65%) during the 4-week period 9 to 12, corresponding to the months of August to November, months after the summer holidays in Spain. Some studies done in the northern hemisphere have observed a higher percentage of cases reported in the months of July, August and September, corresponding to summer holidays (boreal summer) [20‐23]. On the other hand, Pagès et al. [24], analysing cases of imported malaria in Réunion Islands, observed a greater number of cases in the months of January and February, corresponding to summer holidays in the southern hemisphere (austral summer). Therefore, it can be said that the cases of imported malaria are registered mostly after the summer holidays, as it is the season that concentrates the greatest number of movements of the population. Accordingly, clinicians should pay greater attention and actively search for potential travellers prior to these months for advice and chemoprophylaxis.

87.96% of the cases had as causal agent P. falciparum. This percentage resembles what has been observed in other studies conducted in Spain, with 77.46%, 84.1% or 86.43% of imported malaria cases caused by P. falciparum, respectively [7, 8, 10]. The case-fatality rate of malaria cases reported in Aragon from 1996 to 2017 is 0.7%, which coincides with that observed in other studies, between 0.2 and 3% [16, 25]. However, there is no similarity in the percentage of Aragonese cases that required hospital admission, with a high percentage of income (89.3%) compared to 22.1% of Millet et al. [8]. This could be due to the fact that the cases analysed in this study were notified in Reference Units for Tropical Diseases, with better knowledge of malaria management, as well as better access to diagnostic tests and antimalarial treatments. In some Spanish cities, mainly Madrid and Barcelona, there are Reference Units of Tropical Diseases, where people go before and after their tropical travels. These units have their own laboratory, professionals specialized in tropical medicine and the necessary drugs for treatments. Not in all regions of Spain have such facilities. In Aragon, there is an international traveller service consultation for vaccination, but not a reference consultation for diseases after tropical travel. This consultation is carried out in primary care centres or hospital emergencies. The laboratory test for malaria is only available in some hospitals, where hospitalization is often just be done to complete the diagnosis, continuing later outpatient treatment.

Although P. falciparum is the major causative agent in cases of imported malaria in both VFRs, immigrants and travellers, the percentages are different. 93.5% of the infections in the VFR group were caused by this species, with 85.4% among immigrants and 84.8% among travellers. Observing the distribution by continent, 98.7% of VFRs came from Africa, being this percentage lower among immigrants (91.7%) and travellers (84%). This difference in contagion continent may explain the association observed between being VFR and P. falciparum infection, as well as being an immigrant and the infection by other Plasmodium species, since it is in Latin America and Asia where Plasmodium vivax (second most frequent species of Plasmodium among the cases reported in Aragon) is found mostly.

Regarding the presence of fever at diagnosis, 94% of travellers presented it, decreasing to 89.9% in VFRs and 69.4% in immigrants. It has been observed statistically significant association between being VFR and presence of fever, as well as being an immigrant and the absence of it; as in other studies [7, 10]. This could be due to immigrants presenting some degree of semi-immunity against infection, secondary to previous episodes of malaria during their stay in the country of origin. As Phillips et al. [26] observed, travellers to endemic areas of malaria who are exposed to the parasite for the first time, whether children or Europeans without specific immune memory, are more vulnerable and have a higher risk of serious or even fatal malaria. In this sense, the last two mortal cases of malaria in Aragon occurred in a Spanish man who travelled to Guinea for work (2016), and in a 14-year-old boy born in Spain, of Gambian parents, who travelled to see the family for the first time (2017).

It is striking that 74.94% of the cases did not take chemoprophylaxis. This data does not imply the absence of chemoprophylaxis in general, since it is not analysing all VFRs and travellers who have gone to endemic areas, but those who have acquired malaria on that trip. This means that 16.63% of reported cases suffered malaria despite having correctly taken chemoprophylaxis. In other studies, this percentage drops to 8.7% [10]. In addition, in this series, 8.43% took chemoprophylaxis incompletely. Another interesting reading with these data is the high percentage of travellers and VFRs who travel without taking chemoprophylaxis. Only counting the individuals who acquired the infection, we observed a total of 241 cases that did not take it; without having data of all the travellers and VFRs that did not take it, but neither acquired the infection. These data are hopeless, because malaria is a disease that with the correct taking of chemoprophylaxis would greatly decrease its incidence. Roca et al., in a study conducted in the field of primary care with the aim of analysing the knowledge of the immigrant population about the need to receive health advice before travelling to their countries of origin, observed how VFRs do not usually request it because they consider it unnecessary and, when they request it, they frequently address their family doctor in the first instance [9]. Recently, the National Travel Health Network and Centre (NaTHNaC) has seen pharmacists and pharmacies in the UK extend their scope and portfolio to include travel health; moreover, atovaquone/proguanil is available without prescription [27]. Obtaining advice on travel health issues from a pharmacist could be a better option for many, because of the easier access, with flexible appointment times. It would be interesting to adopt this measure in other countries. In Spain, chemoprophylaxis for VFRs is subsidised, with prescription by any doctor of the health system. With the exception of mefloquine, which is dispensed only in the traveller’s consultation (in which there is difficulty of access by waiting list), but free of charge..

95.2% of the cases of malaria reported in Aragon from 1996 to 2017 come from sub-Saharan Africa and, of these, almost half (48.1%) from Equatorial Guinea, Spanish ex-colony. However, the number of foreigners residing in this region of Spain from Equatorial Guinea is clearly lower than that from the rest of sub-Saharan Africa (697 compared to 11,357 in the census on January 1st, 2017) [17]. This evidence has been objectified in the same way in other studies conducted in Spain, with percentages of cases imported from Equatorial Guinea up to 57.1% [8] and 86.26% [7]. In other countries, there has also been a greater number of cases of imported malaria from the corresponding ex-colonies. For example, in France (Marseille) Parola et al. saw a greater number of cases from the Comoros archipelago [12]; in Italy (Milan) Antinori et al. observed the highest percentage of cases from Eritrea [13]; and in Great Britain, Rees et al. found more cases from Nigeria, Ghana and Sierra Leone [14]. This could be due to a greater facility to obtain the nationality, a better knowledge of the language and the sanitary system, or to probable more stable legal and economic conditions. Access to health system in Spain has undergone changes in recent years. At the present time, after Royal Decree-Law 7/2018 [28], emergency assistance is universal, and the necessary requirement to access to public health system is the municipal register (independent of the legal situation). This is controlled by the autonomous communities, which require different minimum registration period to get the health card (most, like Aragon, require 3 months). This means that VFRs have free access to public health system, and newly arrived immigrants only have access to the emergency department until they reach 3 months of registration (for vulnerable groups, there are other specifications in the legislation).

It has been observed a moderate association between Equatorial Guinea and being woman, as well as coming from the rest of sub-Saharan Africa and being man. In the population census of Aragon of January 1st 2017, shows that 63.41% of foreigners from Equatorial Guinea living here are women, compared to 30.04% of women in the group of foreigners from the rest of sub-Saharan Africa [17]. According to United Nations Organization data, female emigration in Equatorial Guinea in 2017 was higher than the male emigration (52.35% versus 47.64%), with Spain being the second country of destination after Gabon. This is the case not only in Equatorial Guinea, as in other African countries such as Democratic Republic of Congo, Côte d’Ivoire, Cameroon, Kenya, Liberia, Namibia or Sierra Leone, female emigration in 2017 was also higher than male migration [29]. Throughout history, migratory movements have been changing. The presence of women in the migration process is increasing [30], and although their social visibility continues to be scarce in relation to the social visibility of immigrant men, research on the feminization of migration is increasing. Women now migrate independently, as the main income generators, instead of migrating accompanying their husbands passively as in the beginning. According to studies, migrant women from sub-Saharan Africa are mostly young and single, migrating in search of work usually from the service sector, such as domestic work and child or elderly care [31]. Despite the fact that female emigration from different African countries is higher than male migration, in Aragon the figures for foreign residents from the rest of sub-Saharan Africa are clearly masculine, unlike Equatorial Guinean figures. The reason for this difference is not known.

This gender distribution between Equatorial Guinea and the rest of sub-Saharan Africa may be the reason for the association between proceeding from Equatorial Guinea and residing in the main province (mostly urban area), as well as between proceeding from sub-Saharan Africa and residing in rural area with important agricultural activity (mainly male activity at present).

The main limitations of this study was the loss of information of the variables reason for travel, fever and chemoprophylaxis in the cases reported in the main province from 1996 to 1999 and in the other provinces from 1996 to 2017. In addition, the epidemiological survey of malaria in Aragon is manual, without mandatory completion of all the variables, in many cases losing data on some of the variables of interest (sometimes probably because of the language barrier).