Background & History
Malaria is caused by five species of intracellular protozoan parasite of the genus Plasmodium, transmitted by mosquitoes of the genus Anopheles. The parasite proliferates through repeated cycles within the red blood cells1 and as these rupture, the infected person displays febrile symptoms including the classic periodic rigors of malaria.2 Morbidity and mortality are greatest in children and also in those adults who are exposed to infection for the first time. Adults who have been frequently exposed to infection since childhood may have strong immunity3 and resistance to the most serious effects of malaria.4
Malaria has been called ‘the king of tropical diseases’ although until 2016 it was transmitted in all World Health Organization (WHO) regions, with about half of the world’s population at risk.5 Plasmodium species are highly adaptable and have occurred in environments as diverse as tropical forests and arctic tundra.6 However, the geographic range of malaria has contracted in recent decades,7 with transmission declared absent from Europe in 2016 and in steep decline in the northern and southern extremities of its range. This former distribution in the temperate and sub-tropical zones has faded from popular memory and malaria is now perceived entirely as a disease of the tropics. All reports of malaria in Europe are considered to be imported, with the rare exceptions of ‘cryptic’ or ‘airport’ malaria and infrequent autochthonous infections, as seen in Greece in recent years.8,9 Currently, the United Kingdom and France report approximately 50% of cases seen in European Union countries.
Most deaths from malaria are due to Plasmodium falciparum, as other Plasmodium species lack P. falciparum’s ability to cause cerebral disease. It should not be assumed that other forms of malaria are trivial or cannot be lethal. Ninety percent of deaths due to malaria occur in sub-Saharan Africa. This makes great demands of countries already facing other major health and social challenges10 and which may have to prioritise use of scarce resources in response.
The global number of malaria cases declined by 18% from 262 million in 2000 to 214 million in 2015. Of the 2015 total, 88% of cases were in the WHO African Region, 10% in the WHO South-East Asia Region (which includes India) and 2% in the WHO Eastern Mediterranean Region. The decline in mortality due to malaria is also important, with a fall of 48% from 2000 (est. 839,000) to 2015 (438,000). In 2015, geographic proportions for mortality were similar to those for case numbers, 90% being in Africa, with 7% in South East Asia and 2% in the Eastern Mediterranean Region. Taking population growth into account, the global mortality rate has fallen by approximately 60% in the last 15 years.
Malaria remains an important cause of illness and death in children under five, but there have been considerable improvements: child deaths from malaria declined by 58% from 723,000 in 2000 to 306,000 in 2015. In the WHO African Region, the number of deaths fell from 694,000 in 2000 to 292,000 in 2015. Nonetheless, malaria accounted for 10% of child deaths in sub-Saharan Africa in 2015. WHO also notes that the proportion of children aged 2 - 10 years infected with Plasmodium sp in sub-Saharan Africa has fallen from 33% in 2000 to 16% in 2015.5
While there are grounds for cautious optimism about the prospects for malaria control in Africa,11 it is in Asia that the most remarkable developments have been made. Countries with previously high malaria endemicity, such as Malaysia and Indonesia, report declining incidence. Sri Lanka has reported no indigenous cases to WHO since 2012.12 In 2014, China reported only 56 autochthonous cases of malaria to WHO, all in the south of the country. Eradication of malaria from China appears to be within reach13 although infection imported from Africa continues to be a cause of concern.14 In 2012 it was noted that the Philippines had recorded a 75% decrease in reported malaria in the preceding ten years15 and this decline has continued due to sustained widespread control interventions.16
There remains a pressing need to maintain progress in control and eradication of malaria in Asia. Climatic conditions will continue to be appropriate for the mosquito vector and it should not be assumed that vector control alone is sufficient to prevent resurgence or re-establishment of malaria.
Drug resistance is an important threat in South East Asia, being identified in Laos, Cambodia, Thailand, Vietnam and Myanmar (Burma). Drug resistance occurs sporadically over a wide geographic range, although it has not become established in all populations of P. falciparum. The possibility of artemisinin resistance in malarious countries with high population such as India17 is a matter of concern, as is the risk of spread to Africa where endemicity has proven most intractable.18
Surveillance and outcomes
Surveillance of malaria in Scotland supports prevention of the disease as it affects travellers to or from malarious countries by collating information on geography, demographics and behaviour associated with risk. Health Protection Scotland (HPS) continuously reviews local, national and international data19 on epidemiology,20,21 outbreaks22 and drug resistance23,24 to produce evidence-based malaria prevention guidance in conjunction with the Scottish Malaria Advisory Group. This guidance, with accompanying maps, is published on TRAVAX (http://www.travax.nhs.uk) and fitfortravel (http://www.fitfortravel.nhs.uk).
Countries for which new guidance and maps have recently been published by HPS include Malaysia (2015), Nepal (2015), China (2016), Vietnam (2016) and Cambodia (2016).
Scottish malaria data is monitored to ensure relevance and quality. Since 2013,25 all malaria specimens are referred to the Scottish Parasite Diagnostic and Reference Laboratory (SPDRL) for confirmation and follow-up. Data on age, sex, diagnosis, parasite species, country of origin, travel, prophylaxis and ethnicity are routinely collated. Only speciated reports confirmed by PCR or microscopy are included in the data.
The Scottish data is submitted to the Malaria Reference Laboratory (MRL) in London which collates all data on malaria imported into the United Kingdom. Any reports from Scotland where the patient has given a UK address outwith Scotland are allocated to the appropriate part of the UK, and likewise any Scottish residents diagnosed elsewhere are allocated to Scotland. The Scottish data for the period 2015 cited above was analysed using Microsoft Excel.
In a change from previous years, this report considers the three most recent years’ Scottish data. The United Kingdom malaria report for 2015 will be published later and will not be referred to here.
Malaria in Scotland, 2015: results
In 2015, there were 49 reports of malaria in Scotland, 35.5% lower than 2014 (N=76) and 16.9% lower than 2013 (Figure 1).
Age and sex were recorded for all 49 individuals with 67.3% male (N=33) and 32.7% female (N= 16) (Figure 2). Mean age for all reports was 39.7 years (SE 2.1). Mean age for females was 37.0 years (SE 3.7) and for males 41.0 years (SE 2.6). Reports peaked at 35 – 39 years for females (N=3) and at 40-44 years for males (N=7). Peak age groups for total reports was 40-44 years (N=8).
P. falciparum was the most common species at 83.7% (N=41) followed by P. vivax at 10.2% (N=5). Three (6.1%) infections were identified as P. ovale. (Figure 1).
No deaths from malaria were reported in Scotland in 2015.
Region and country of transmission
Region of transmission was recorded for 89.8% (N=44) of Scottish reports (Table 1). Africa accounted for 84.1% (N=37) of these with 64.9% (N=24) coming from West Africa. Within West Africa, most reports originated from Nigeria 45.8% (N=11), Ghana 20.8% (N=5) and Sierra Leone 16.7% (N=4). The proportion from East Africa was 16.3% (N=8). Within East Africa, 37.5% (N=3) came from Kenya, 25.0% (N=2) from Uganda, 25.0% (N=2) from Sudan and 12.5% (N=1) from Eritrea. Central Africa provided 11.4% (N=5) of reports where region of transmission was recorded. Within this region, three (60.0%) came from Congo and one (20.0%) each from Cameroon and Central African Republic. Four (9.1%) reports where region was reported came from Southern Africa. Of these, three (75.0%) came from Angola and one (25%) from Zambia. One report (2.3%) came from Asia (Pakistan) and one (2%) came from South America (French Guiana).
Region of transmission was recorded for 87.8% (N=36) reports of P. falciparum, of which 61.1% (N=22) came from West Africa. Southern, East and Central Africa each contributed 11.1% (N=4) of P. falciparum reports where region was recorded. One report (2.8%) of P. falciparum came from Asia (not South East or Far East). Region of transmission was recorded for all five reports of P. vivax. Three (60.0%) of these came from East Africa, one (20.0%) from West Africa and one (20.0%) from Central and South America.
Reason for travel
Thirty-six individuals (73.5%) gave a reason for travel (Table 2). Visiting friends & relatives (VFR) accounted for 33.3% (N=12) of these, while 25.0% (N=9) were business/professional travellers. Four (11.1%) were new entrants to the UK. There were three (8.3%) holiday travellers and three (8.3%) foreign students. Two (5.6%) were recorded as foreign visitors and two (5.6%) were UK citizens abroad. One report (2.8%) was a UK serviceman.
People of Black African ethnicity (N=20) and African descent (N=5) comprised 45.5% and 11.4%, respectively, of the 44 whose ethnicity was specified (Table 3). Thirteen individuals (29.5%) were recorded as White British. Those recorded as Other White ethnicity comprised 6.8% (three) of reports where ethnicity was specified. Mixed ethnicity and Indian Subcontinent were 4.5% (N=2) and 2.3% (N=1) respectively.
Twenty-three (46.9%) individuals did not specify if chemoprophylaxis was used (Table 4). Twenty (76.9%) of the remaining 26 specified chemoprophylaxis reported that they took no chemoprophylaxis while four (15.4%) took doxycycline and two (7.7%) reported they took mefloquine. One individual reported taking chemoprophylaxis regularly. This amounts to 2.0% of the malaria reports for 2015.
Malaria in Scotland, 2013-2015: results
In the three years from 2013 to 2015, there were 184 reports of malaria in Scotland. There were 59 (32.1%) reports in 2013, 76 (41.3%) reports in 2014 and 49 (26.6%) reports in 2015 (Figure 1).
Age and sex were recorded for 99.5% (N=183) of these, 73.3% (N=129) being male and 26.7% (N=54) being female. Mean age for males was 38.3 years (SE=1.3) and for females 33.9 years (SE=2.0). Age distribution peaked at years 25-29 years for females (N=9) and at 40-44 for males (N=18). Peak age for total reports was 25-29 (N=25) (Figure 3).
P. falciparum accounted for 142 reports (77.2%), while 15.2% (N=28) were P. vivax. P. ovale at 3.8% (N=7) and P. malariae at 2.7% (N=5) were less frequently seen. There were two (1.0%) mixed infections of which one was P. falciparum / P. malariae and one was P. falciparum / P. vivax (Figure 1).
There was one death from P. falciparum in Scotland in 2013.
Region and country of transmission
Region of transmission was recorded for 178 (96.7%) reports (Table 5). Of these, West Africa contributed 53.4% (N=95), East Africa 12.9% (N=23) and Asia (not Far East or South East) 12.4% (N=22). Within West Africa, Nigeria and Ghana contributed the greatest number, with 43.2% (N=41) and 14.7% (N=14) respectively. In Asia, Pakistan 68.2% (N=15) was the source of most reports, with India contributing 31.8% (N=7).
Region of transmission was recorded for 95.8% (N=136) reports of P. falciparum, of which 63.2% (N=86) came from West Africa. Southern Africa and Central Africa contributed 12.5% (N=17) and 10.3% (N=14) respectively. East Africa provided 9.6% (N=13) and 3.7% (N=5) came from Asia, the Far East and South East Asia and Oceania collectively.
Region of transmission was recorded for 100% (N=28) reports of P. vivax. Of these, Asia (not South East or Far East) contributed 64.3% (N=18). East Africa provided 25.0% (N=7) of P. vivax reports. One report (3.6%) came from each of Oceania, Central & South America and West Africa.
Reason for travel
In the 80.4% (N=148) reports where a reason for travel was given, VFR was commonest at 35.1% (N=52). This was followed by business/professional travel 23.6% (N=35), holiday travel 12.8% (N=19), and foreign students 8.1% (N=12). New entrants to the UK contributed 7.4% (N=11). (Table 6).
Ethnicity was recorded in 170 reports. Of these, 48.2% (N=82) were of Black African or of African descent, 37.6% (64) were White British or Other White. 10.0% (N=17) recorded their ethnicity as Indian Subcontinent or Indian/Pakistani/Bangladeshi descent. Other Asian was 2.4% (N=4) and Mixed Ethnicity was 1.8% (N=3) (Table 7).
In total, 19% (N=35) reported taking chemoprophylaxis, of whom 57.1% (N=20) took doxycycline, and 22.9% (N=8) took atovaquone/proguanil. Four (11.4%) reported taking mefloquine. The remainder comprised 2.9% (N=1) primaquine, 2.9% (N=1) chloroquine and 2.9% (N=1) unidentified chemoprophylaxis. Of the 35 where chemoprophylaxis was reported, 20% (N=7) reported taking it regularly. This amounts to 3.8% of all malaria reports for 2013-2015 (Table 8).
Overview of surveillance
Malaria numbers in Scotland fluctuate annually and 2015 is no exception. Reporting numbers tend to reflect patterns of travel or transmission elsewhere.26 As surveillance is historical in nature, apparent changes in reporting indicate conditions in the immediate past, and are not by themselves indicative of the current risk, or that of the near or more distant future. It is therefore important to examine malaria occurrence over a number of years to gain a clearer idea of the epidemiology and risk of infection, particularly in those countries with unstable or epidemic malaria.
The introduction of enhanced surveillance of malaria in Scotland has led to an improvement in data quality, with a preliminary consideration of the first three years of data presented here. It is envisaged that the data will become more useful as additional material is recorded in subsequent years.
The Scottish data set for 2015 is similar to previous years. The great majority of reports are of infection acquired in Africa, with West Africa remaining the main source of malaria imported from that continent. Nigeria is again the biggest contributor of any country, with Ghana and Sierra Leone ranking second and third, respectively.
Most malaria in Africa is P. falciparum and this is reflected in the Scottish data for 2015, as well as in the data for 2013-2015, which is consistent with historical records. P. vivax is recorded far less frequently in Scotland, despite its great geographical range and occurrence in countries such as Pakistan which receive many visitors from Scotland. While P. vivax is the dominant form of malaria in much of the world outside Africa, it is in decline over much of its range, particularly in South East Asia and the Far East. Consequently, travellers to P. vivax endemic areas may encounter a weaker force of infection than in Africa, perhaps for a short period of time, in conditions not conducive to infection in the visitor or temporary resident. There is also the possibility that Scottish travellers to some P. vivax-endemic countries such as Pakistan may be there for weeks to months, with disease being diagnosed and treated before return home. However, if this were the case it might be expected that relapsing P. vivax might be reported more often in Scotland and there is little evidence of this occurring.
Groups at risk
Risk of malaria derives from a complex set of characteristics that varies according to the individual traveller and conditions of exposure. Two important characteristics are region of travel and type of traveller, with the ethnicity of the traveller having a strong influence on both of these. The UK malaria report for 201412 noted that 70% of the UK dataset is Black African and of non-White British travellers, 94% being VFR travellers. In the 2013-2015 Scottish reports, 41 (78.8%) of 52 VFR travellers identified as Black African or of African descent.
In 2015, where ethnicity was recorded, 45.5% of reports were in people whose ethnicity was recorded as Black African, with a further 11.4% being reported as of African Descent. Those recorded as White British were 29.5% of the reports where ethnicity was recorded, with another 6.8% being of Other White background. White British travellers diagnosed with malaria in Scotland for the past three years account for 33.5% of those whose ethnicity was recorded, indicating malaria risk is not only a challenge for those whose recent heritage lies in malarious countries.
The 2015 Scottish figures indicate 69.4 1% (N=25) had travelled abroad from Scotland/UK while 30.6% (N=14) had begun their journeys abroad, these proportions compared to three-year figures of 75.0% (N=111) and 25.0% (N=37) respectively.
It is important to note that only six (24.0%) of the 25 who travelled abroad from Scotland in 2015 reported taking chemoprophylaxis and only one (17%) of these confirmed that it had been taken regularly. In the years 2013-2015, 27.0% (N=30) of those diagnosed with malaria and whose journeys began at home reported that they took chemoprophylaxis. Only six (20%) of these stated that they took the medication regularly. These observations support the link between diagnosis of malaria and the failure to take antimalarial chemoprophylaxis correctly, or to take it at all. While it is important that chemoprophylaxis is appropriate to the country visited, it is hard to find evidence of true failure of chemoprophylaxis in the Scottish data. Thus, it remains essential that travellers are given not only appropriate advice, but that they have a clear understanding of what is required to prevent malaria and that they follow the necessary processes. PHE noted that, of malaria patients who had travelled abroad from the UK in 2014 and had been questioned on the subject, 82% had taken no antimalarial chemoprophylaxis.27
While P. falciparum remains endemic in most of sub-Saharan Africa, it is likely that travellers to and from Africa will continue to form a large proportion of reports in the Scottish data set. VFR travelers are once again a noteworthy group within those travelling from Scotland. These travellers may have a misplaced belief in their innate immunity or the safety of their destination and thus disregard adequate prevention. Similarly, students returning home to malarious countries may disregard risk if they have not experienced serious malaria for a lengthy period of time due to immunity acquired since childhood.28 However, immunity wanes quickly without exposure, placing travellers at risk if they return home after months away.
However, business travellers and UK citizens abroad together form another important group. Business travellers may depart at short notice without adequate preparation, knowledge or appropriate advice. Some longer term business travellers and UK citizens abroad may form a similar group to new entrants from endemic countries in that they may have high exposure to infection and may neglect chemoprophylaxis and use medication only in the event of clinical malaria.
Healthcare providers are urged to alert members of such groups to the malaria risks involved, particularly where travellers are pregnant or travelling with children. The possibility of malaria should always be considered in a febrile patient arriving from a malarious country,29 whether or not the patient belongs to a perceived high-risk group. It remains important that clinicians should be aware of the possibility of malaria, particularly in members of refugee communities arriving from Africa.
Malaria from Africa
Africa remains the largest source of malaria reported in Scotland. P. falciparum remains widespread in Africa south of the Sahara and north of the Transvaal, so its occurrence in travellers is unsurprising in epidemiological terms but medically highly significant. Four reports of P. vivax from Africa were submitted in Scotland in 2015. Three of these were from East Africa, from where most African P. vivax originates, often in refugee communities.30,31,32 However, the other African P. vivax reportedly came from Sierra Leone, which is an exceptional rarity. The patient was of White British origin, which is consistent with susceptibility to P. vivax, although it is unusual for anyone to be exposed to this species in West Africa. In such cases, the patient’s travel history requires thorough examination to clarify the origin of infection. Furthermore, consideration of the improbable may be necessary in order to reach a diagnosis.
There was also an unusual report of P. falciparum from South Africa in 2015. Malaria occurs only in the far north of South Africa and it is important to ascertain whether the patient has been in neighbouring countries such as Mozambique where malaria is more common.
Asia, including South East and Far East
Asia is discussed here, as its absence from the reports is noteworthy. In Scotland in 2015, only one report of malaria acquired in Pakistan was received. This was the only report arising from 31,000 visits to India and Pakistan combined that originated in Scotland in 2015.34 Most malaria in much of Asia is P. vivax, which is often refractory to chemoprophylaxis,35 and the epidemiological trend is declining, so the need for chemoprophylaxis is variable.36 In the past decade, reports of malaria from Asia beyond the Indian subcontinent have been rather infrequent in the UK reports. Indeed, there is only one report from the Far East and South East Asia in the three-year data set discussed here. Nonetheless, P. falciparum is widespread and must be considered as part of a targeted risk assessment. Incidence within Asian countries is often highly variable and creation of appropriate guidelines a potentially complex process.
In parts of South East Asia, the zoonotic P. knowlesi has replaced P. falciparum to become the main cause of severe or fatal malaria. This should always be considered as part of risk assessment for travellers to rural or peri-urban areas in endemic countries where incidence of P. knowlesi may be poorly recorded.
HPS is currently revising malaria prevention guidelines for Asia. This work began with India, but has expanded to include most of South East Asia and the Far East. Some of these revisions are already published and others will be launched on TRAVAX and fitfortravel once finalised. In some areas where chemoprophylaxis was previously always recommended, bite avoidance, prompt diagnosis and treatment are now preferred. Withdrawal of the chemoprophylaxis recommendation for large areas of India and some other Asian countries is predicated on evidence that incidence in residents and travellers is sufficiently low as to present limited risk to visitors who practise effective bite avoidance.
Malaria in Latin America and the Caribbean
In 2015, one episode of P. vivax malaria from French Guiana (France) was reported in Scotland. That this was the first such report in Scotland in recent years and its rarity may derive from small visitor numbers37 and a decline in malaria in South and Central America.5 There have been no other reports of malaria imported into Scotland from South America since enhanced surveillance began. The episode reported here is of interest for its geographical origin and the fact that the patient is recorded as having taken chemoprophylaxis, which can be consistent with suppression of initial illness and failure to prevent relapse. Where P. vivax is prevalent, effective bite avoidance should be considered an essential form of prevention. HPS has recently carried out a re-assessment of malaria in Panama, Guatemala and Honduras and this has demonstrated strongly declining risk in these countries. However, low or declining level of risk in a malarious country does not mean precautions are unnecessary, rather that the nature of the required precautions may change.
Public awareness of chemoprophylaxis
During 2015 concerns about the safety of chemoprophylaxis using mefloquine were raised as a result of parliamentary investigations into the effects of its use by members of the British armed forces.37 While campaigning and debate about its potential to cause adverse effects38 are likely to continue in the UK and elsewhere, mefloquine remains a valuable drug to be used in appropriate settings following thorough risk assessment based on context and contraindications.39,40
Advice to travellers
The Scottish malaria reports for the last three years confirm the importance of appropriate chemoprophylaxis: where this is taken as directed, the risk of malaria is small. The risks associated with VFR travel, particularly to Africa, are further confirmed. Travellers from Scotland visit malarious areas in considerable numbers each year.26 Some travel for leisure and business and the diversity of the population means many are VFR travellers. Travellers to malarious countries should always seek pre-travel evidence-based advice from specialist health professionals and be aware of the malaria risk associated with specific intended destinations. TRAVAX (http://www.travax.nhs.uk) provides travel health professionals with evidence-based guidance for travellers.41,42
All travellers should follow the ‘ABCD’ of malaria prevention.
A--be Aware of the risk
B--prevent mosquito Bites
C--take appropriate Chemoprophylaxis if required (or advised)
D--early Diagnosis can be life-saving.
HPS would like to thank the Public Health England Malaria Reference Laboratory for collating and supplying data, and also the various laboratories in Scotland who have contributed enhanced data.
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- Andriopoulos P, Economopoulou A, Spanakos G, Assimakopoulos G. A local outbreak of autochthonous Plasmodium vivax malaria in Laconia, Greece - a re-emerging infection in the southern borders of Europe? International Journal of Infectious Diseases 2013;17:e125-e128. Available from: http://www.sciencedirect.com/science/article/pii/S1201971212012623. (accessed 7 July 2016).
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- Gething PW, Battle KE, Bhatt S et al. Declining malaria in Africa: improving the measurement of progress. Malaria Journal. 2014;13:39. Available from: https://malariajournal.biomedcentral.com/articles/10.1186/1475-2875-13-39. (accessed 7 July 2016).
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