Background and history
Malaria occurs in all WHO regions, with about half of the world’s population at risk and 1.2 billion at high risk.1 It is caused by five species of intracellular protozoan parasite of the genus Plasmodium, transmitted by mosquitoes of the genus Anopheles. The hepatocytes are infected first and the parasite progresses through repeated proliferative cycles within the red blood cells.2 As the red cells rupture, the infected person displays febrile symptoms including the classic periodic rigors of malaria.3
Malaria has retreated towards the tropics in recent decades,4 although transmission continued up to 1973 in the Netherlands, where some of the most important studies of relapse in Plasmodium vivax were conducted.5 Plasmodium is an adaptable organism and has occurred in environments as diverse as tropical forests and arctic tundra.6 All malaria within the European Economic Area (EEA) is identified as imported, with sporadic exceptions of ‘cryptic’ cases and rare autochthonous infections as recently seen in Greece.7,8
The greatest burden of malaria rests on sub-Saharan Africa,where 90% of malaria deaths occur, mostly due to P. falciparum. This makes great demands of countries that face other major challenges.9 In 2013, Sierra Leone reported 1.7 milion cases and 4326 deaths from malaria to WHO.1 The following year, in addition to the annually-occurring burden of malaria and other infections, Sierra Leone reported 9446 cases of Ebola virus disease (EVD), including 2758 deaths.10 During the EVD epidemic, the challenges presented by malaria continued, with some patients unable to obtain treatment due to healthcare providers’ fear of exposure to Ebola virus, or failure of the public health infrastructure. A recently published mathematical model indicated there could be 3.5 million additional untreated cases of malaria with 10,900 deaths in Guinea, Liberia and Sierra Leone in 2014 due to failure of malaria treatment provision.11 In a move to mitigate the disruption of malaria treatment by the EVD epidemic, Médecins Sans Frontières distributed 1.8 million malaria treatments in Sierra Leone in January 2015.12
Prospects for control and eventual eradication of malaria give cause for cautious optimism. Global funding has expanded in recent years, facilitating vector control and escalation of diagnostic testing. Delivery of preventive therapies and access to treatment with artemisinin-based combination therapies is improving. However, there are still significant gaps in intervention and resistance to antimalarial drugs remains challenging.
Some Asian countries with historically high malaria endemicity, such as Malaysia and Indonesia, report declining incidence. Sri Lanka reported no indigenous cases to WHO in 2013. Furthermore WHO reported in 2014 that malaria prevalence has fallen across sub-Saharan Africa, particularly Central Africa, since 2000. Average infection prevalence in children (2–10 years) fell by 46% from 26% in 2000 to 14% in 2013. The number of people infected with Plasmodium sp at any one time across Africa fell by 26% from 173 million in 2000 to 128 million in 2013. If the annual rate of decrease is maintained, by this year malaria mortality has been projected to decrease by 55% globally and by 62% in Africa. Malaria mortality in children aged under five is predicted to fall by 61% globally and by 67% in Africa.1
Surveillance of malaria in the UK aims to support prevention of the disease as it affects travellers to or from malarious countries by collating information on geography, demographics and behaviour associated with risk.13,14,15 Health Protection Scotland (HPS) continuously reviews from local, national and international data16 on epidemiology,17,18 outbreaks19 and drug resistance20,21 to produce evidence-based malaria advice with accompanying maps published on TRAVAX (http://www.travax.nhs.uk) and fitfortravel (http://www.fitfortravel.nhs.uk). The Scottish Malaria Advisory Group, of which HPS is partner, has recently provided updated evidence-based malaria prevention advice for travellers to Indonesia (2014), Sri Lanka (2014), Malaysia (2015) and Nepal (2015).
Annual Scottish malaria data is monitored to ensure relevance and quality. Since 2013, it is required,22 that all malaria specimens are referred to the Scottish Parasite Diagnostic and Reference Laboratory (SPDRL) for confirmation and follow-up. In addition to routine data on age, sex and diagnosis, data on parasite species, country of origin, travel, prophylaxis and ethnicity are collated to form the enhanced data set. The Scottish data are submitted to the Malaria Reference Laboratory (MRL) in London which collates all data on malaria imported into the United Kingdom. The MRL dataset including the HPS data for the period 2014 cited above was analysed using Microsoft Excel.
2014 United Kingdom data
In 2014, there were 1586 reports of malaria in the United Kingdom, an increase of 5.7% on 2013 (N=1501) (Figure 1).
Age and sex were recorded for 1582 individuals with 68.5% male (N=1083) and 31.5% female (N= 499) (Figure 2). These proportions are similar to previous years. Mean age for males was 38.3 years (SE=0.5) and for females 37.0 years (SE=0.8). One hundred and fifty three individuals (9.6%) were aged sixteen or under. Reports peaked at 45-49 years for males (N=135) and at 40-44 years for females (N=62) (Figure 2). Peak age group for total reports was 45-49 years (N=189).
P. falciparum was the most common species at 73.7% (N=1169) followed by P. vivax at 14.2% (N=225), while 8.2% (N=130) were identified as P. ovale. Twelve (0.8%) were mixed P. falciparum / P. ovale, five (0.3%) were mixed P. falciparum / P. malariae and three (0.2%) were mixed P. falciparum / P. vivax. One (0.1%) was identified as mixed P. vivax / P. knowlesi. Added to the P. vivax and P. ovale reports, this gives a total of 23.4% (N=371) reports with potential for relapse. Forty-one reports (2.6%) were P. malariae.
Three individuals (0.2%) whose ages ranged from 54 to 83 years died due to P. falciparum from Nigeria.
Region of transmission
Region of transmission was recorded for 92.8% (N=1472) of UK reports (Table 1). Africa accounted for 87.5% (N=1288) of these with 72.3% (N=931) of African reports coming from West Africa. Within West Africa, most reports originated from Nigeria 54.7% (N=509), Ghana 16.5% (N=154) and Sierra Leone 13.7% (N=128). The portion from East Africa was 10.9% (N=160). Most of these came from Uganda 26.9% (N=43), Kenya 20.6% (N=33), Eritrea 15.0% (N=24) and Sudan 14.4% (N=23). Thirty-seven (23.1%) P. vivax infections (including two mixed P. falciparum/P. vivax) came from East Africa. Asia (not South East or Far East) contributed 10.9% (N=161). Of these, most reports were from Pakistan 62.1% (N=100) and India 31.7% (N=51).
Twelve reports (0.8%) originated in Central & Latin America. The Far East & South East Asia contributed 0.4% (N=6). Three (0.2%) reports came from Oceania while the Middle East and Caribbean contributed one (0.1%) report each.
Reason for travel
Reason for travel was recorded for 71.0% (N=1126) of reports (Table 1). ‘Visiting friends and relatives’ (VFR) accounted for 60.6% (N=682) of these. Young people (aged 16 or younger) accounted for 9.8% (N=67) of the VFR group. VFR was followed by business & professional travel 9.5% (N=107), foreign visitors to the UK 9.4% (N=106), new entrants to the UK 8.2% (N=92) and holiday travellers 5.9% (N=66).
2014 Scottish data
There were 76 reports of malaria in Scotland, equivalent to 4.8% of the UK total (Figure 1). This is an increase of 28.8% since 2013 (N=59), and is higher than the UK increase of 5.7%. Age and sex were recorded for all individuals, of whom 75.0% (N=57) were male and 25.0% (N=19) were female (Figure 3). Mean age for males was 37.4 years (SE=2.0) and 30.79 years for females (SE=3.1). Four individuals were aged 16 or under. Age distribution for males peaked at 20-24 years (N=10) and at 50-54 years (N=9). Peaks for females were at 20-24 years (N=4) and 45-49 years (N=4).
Reason for travel
A reason for travel was given by 64 individuals (84.2%) (Table 2). VFR accounted for 28.1% (N=18) of these, while 23.5% (N=15) were business/professional travellers. Ten (15.6%) were holiday travellers, while 9.4% (N=6) were foreign students. New entrants, foreign visitors and UK citizens abroad comprised 6.3% (N=4) each. Civilian sea/air crew and British armed forces amounted to 4.7% (N=3).
Region of transmission
Region of transmission was recorded for 98.7% (N=75) Scottish reports (Table 2). Of these, 68 (90.7%) came from Africa and 40 (58.8%) specifically from West Africa. Southern Africa contributed 14.7% (N=10). East Africa and Central Africa each contributed 13.2% (N=9) of African reports. Six reports (8.0%) were from Asia and one was from Oceania (1.3%).
Of the 76 reports, 61 (80.2%) were P. falciparum and eight (10.5%) were P. vivax. P. malariae 5.3% (N=4) and P. ovale 1.3% (N=1) made up the remainder of single-species infections. Two (2.6%) were mixed infections, of which one was P. falciparum/P. vivax and the other P. falciparum/P. malariae.
2010-2014 Scottish data
In the five years from 2010 to 2014, there were 310 reports of malaria in Scotland (Figure 4). Age and sex were recorded for 97.7% (N=303) of these, of which 73.3% (N=222) were male and 26.7% (N=81) were female. Twenty (6.6%) were aged sixteen years or under. Mean age for males was 35.8 years (SE=1.0) and for females 32.4 years (SE=1.7). Age distribution peaked at 25-29 years for both males (N=40) and females (N=14).
Two hundred and nine (67.4%) were P. falciparum while 22.6% (N=70) were P. vivax. P. ovale at 6.5% (N=20) and P. malariae at 2.3% (N=7) were less frequently seen. There was one (0.3%) P. knowlesi. There were three (1.0%) mixed infections of which one was P. falciparum/P. malariae, one was P. falciparum/P. ovale and one was P. falciparum/P. vivax.
Region of transmission
Region of transmission was recorded for 242 (78.1%) reports (Table 4). Of these, West Africa contributed 50.8% (N=123), Asia (not Far East or South East) 18.6% (N=45) and East Africa 10.7% (N=26). Within West Africa, Nigeria and Ghana contributed the greatest number, with 49.6% (N=61) and 15.4% (N=19) respectively. In Asia, Pakistan 62.2% (N=28) was the source of most reports, with India contributing 35.6% (N=16).
Region of transmission was recorded for 79.9% (N=167) reports of P. falciparum, of which 63.5% (N=106) came from West Africa. Southern Africa and East Africa contributed 13.2% (N=22) and 10.8% (N=18) respectively. Central Africa provided 8.4% (N=14) and 3.0% (N=5) came from Asia and Oceania collectively. Region of transmission was recorded for 70% (N=49) reports of P. vivax. Of these Asia contributed 81.6% (N=40). Africa provided 16.3% (N=8) of P. vivax reports where region was specified. One report (2%) came from Oceania.
Reason for travel
Of the 63.2% (N=196) reports with a reason for travel, VFR was commonest at 37.8% (N=74). (Table 3) This was followed by business/professional travel 21.9% (N=43), holiday travel 12.8% (N=25), and foreign students 10.7% (N=21). Foreign visitors and new entrants to the UK contributed 6.1% (N=12) and 5.1% (N=10) respectively.
Overview of surveillance
Malaria numbers in the UK have fluctuated in recent years and the 2014 total is the second consecutive annual increase.23 This may reflect changing conditions within source countries24 as well as travel and relationships between countries. A recent change in reported numbers in the UK alone does not indicate a changing risk to travellers. The roll-out of enhanced surveillance of malaria in Scotland has seen an improvement in data quality. Ethnicity data has only been recorded consistently in Scotland in 2013 and 2014, so a five-year total for that indicator was not considered here.
The UK and Scottish data sets for 2014 are unsurprising when compared to previous years. West Africa remains the largest source of malaria, with Nigeria making the biggest contribution again. Ghana provides the second largest number of reports in the UK, with Sierra Leone ranking third. In 2013, Sierra Leone provided the second highest number of reports and the decline in 2014 may be due partly to a fall in travel between the UK and Sierra Leone in the context of the EVD epidemic.
Most malaria in Africa is P. falciparum. The PHE report for 201413 noted that where ethnicity is recorded, 70% of the UK dataset is Black African and of all non-White British travellers, 94% are VFR travellers. Only 15% of those whose ethnicity was recorded were described as ‘White British’. Scotland has ethnicity figures for only two years and these will be considered more fully at a later date. However, Scotland had a higher proportion of malaria (38.0%) reported in ‘White British’ patients in 2014, although 49.3% were African with 45.7% of these being VFR travelers. This may be due to differing population composition in Scotland, but the high proportion of White British travelers merits consideration. The 2014 figures indicate 78.1% (N=50) had travelled abroad from Scotland and 21.9% (N=14) had begun their journeys abroad, so targeting advice at this group remains a valid and necessary approach. PHE noted that in 2014, 82% of malaria patients who had travelled abroad from the UK had taken no antimalarial chemoprophylaxis (among those from whom this information was obtained).
Enhanced surveillance during the Commonwealth Games
Glasgow was host to the Commonwealth Games in August 2014, during which event HPS implemented enhanced surveillance of infectious diseases. One report of malaria in Scotland (P. falciparum, Papua New Guinea) was associated with participation in the Games.
Groups at risk
Risks faced by business travellers may be linked to travel at short notice with lack of preparation and appropriate advice. VFR travellers may have a belief in innate immunity or the safety of their destination and thus disregard adequate prevention. Students from malarious countries may also disregard risk if they have not experienced serious malaria for a lengthy period of time due to the acquired immunity achieved through regular exposure to malaria parasites.25 However, this acquired immunity wanes rapidly in the absence of exposure, placing students at risk if they return home during academic holidays. Healthcare providers are encouraged to advise these groups of the malaria risks faced, particularly if travellers are pregnant or travelling with children.
The possibility of malaria should always be considered in a febrile patient arriving from a malarious country, whether or not the patient belongs to a perceived high risk group.
Asia (not Far East or South East Asia) contributes a large minority of infections reported in the UK and Scotland. Pakistan contributes most reports from this region, while India remains visible in the UK records. However, no malaria was reported arising from the 35,000 visits26 to India beginning in Scotland in 2014. Most malaria in Asia is P. vivax, and the epidemiological trend is declining, so the need for chemoprophylaxis is variable.27 Nonetheless, P. falciparum is widespread and must be considered as part of a targeted risk assessment.
Chemoprophylaxis suppresses the primary episode of illness in P. vivax but relapse may occur where hypnozoites have been formed, as these are refractory to most antimalarials.28 In recognition of this, and because the risk of adverse effects can exceed that of malaria, HPS has developed more nuanced guidance for some Asian countries where incidence is low and P. vivax is common. In some areas where chemoprophylaxis was previously always recommended, bite avoidance, prompt diagnosis and treatment are now preferred. Despite withdrawal of chemoprophylaxis for much of India, only two reports (both P. vivax) from India were seen in Scotland this year, both individuals being residents of India.
Plasmodium vivax has been described misleadingly as ‘benign tertian’ malaria. While P. vivax is less often deadly than is P. falciparum, it may still cause serious illness.29,30 All forms of malaria are more dangerous to children and the elderly and there have been deaths from P. vivax in the UK since 2010.31,32 P. vivax is one of two relapsing forms of malaria and may cause recurring bouts of debilitating illness.33 Treatment with primaquine ends the relapse process by eradicating hypnozoites from the liver, but may be contraindicated due to the drug’s ability to cause severe haemolysis in glucose-6-phosphate dehydrogenase (G6PD) deficient individuals.34
P. knowlesi in South East Asia
The limited effectiveness of chemoprophylaxis against P. vivax does not entirely rule out its use where that species is common. The risk of severe malaria in South East Asia is far smaller than in Africa, but the distribution of P. vivax in South East Asia overlaps with that of P. falciparum and P. knowlesi, so the possibility of dangerous illness remains part of the HPS country assessment for that region. It has become apparent that the zoonotic P. knowlesi is more common in South East Asia than previously recognised, though it is rare in western travellers and has been seen only once in Scotland.35 P. knowlesi is usually found in macaques36 and may replace P. falciparum as the main cause of severe malaria in humans. P. knowlesi is difficult to identify microscopically, with young trophozoites appearing similar to those of P. falciparum and mature trophozoites often misdiagnosed as P. malariae.37 One study showed P. knowlesi accounted for 59% of 107 PCR-positive results in a total of 243 blood spot samples submitted for malaria identification, with no P. malariae identified in the study.38
Evidence from Malaysian Borneo shows that P. knowlesi is now the most common malaria in Sabah39 just as malaria enters the eradication phase in Malaysia. P. knowlesi is enzootic in monkey populations which has implications for its control in areas where malaria is in decline, but where monkeys come into contact with humans. Its presence in forest areas presents a risk to travellers as exemplified by a mixed P. knowlesi/P. vivax infection from Malaysia in the UK reports in 2014.
P. vivax in Africa
P. vivax occurs in a minority of African reports due to the rarity of the Duffy blood antigen in west and central Africa.40 The Duffy blood antigen is the cell receptor usually required by P. vivax for red cell entry, so where it is rare, P. vivax tends to be uncommon or absent. However, some P. vivax is able to exploit more than one host receptor.41 In some areas of Africa where there is Duffy-positive migration, there may be a sufficiently large and diverse parasite population, some of which has the ability to infect Duffy-negative people.42,43,44 P. vivax has been seen in Eritrean migrants outside East Africa in recent years45,46,47 with four reports linked to Eritrea in Scotland in 2014. Nearly one quarter of the malaria reported from East Africa in the UK in 2014 was P. vivax. Malaria influences48,49 and responds50 to socio-economic, military and political events. Breakdown in infrastructure and control can lead to an upward epidemiological trend which may be seen in neighbouring countries as populations spill across borders.51
Advice to travellers
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.52,53
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 wish to thank the Public Health England Malaria Reference Laboratory for collating and supplying data, and also the various laboratories in Scotland who have supplied enhanced data to Health Protection Scotland.
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- Walker PGT, White MT, Griffin JT et al. Malaria morbidity and mortality in Ebola-affected countries caused by decreased health-care capacity, and the potential effect of mitigation strategies: a modelling analysis. Lancet Infectious Diseases. 2015;15:825-32. Available from: http://www.thelancet.com/journals/laninf/article/PIIS1473-3099(15)70124-6/fulltext. (accessed 22 July 2015).
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