Surveillance of travel-related infections tends to focus on diagnoses in tourists, people visiting friends and relatives, or those returning from business trips. In 2016, these areas of travel have remained significant in terms of travel health, with some noteworthy developments. The growing outbreak of Zika virus disease across the tropics and subtropics, notably in the Americas, was accompanied by an increase in neurodevelopmental defects and other pathology in babies born to mothers who had been infected with Zika virus while pregnant.
As well as surveillance, the Zika virus outbreak required development of advice to travellers before and after travel1 and development of monitoring processes for women who might have been exposed to infection while pregnant.
These developments stood in contrast to the previous response to the Ebola virus disease epidemic in west Africa of 2014-2015, where the main aim was to prevent importation and spread of a highly contagious and virulent pathogen. Such a scenario was highly unlikely where Zika virus is concerned, as the United Kingdom does not have the Aedes mosquito vector necessary for transmission of the virus. However, as a Public Health Emergency of International Concern (PHEIC) had been declared on the basis of what was not known about Zika virus, it was appropriate to take steps to prevent infection of travellers, and any children they might have subsequent to their journey.
More generally, infections acquired during travel may have the potential for transmission in transit or when the traveller arrives home or at another destination, although this potential is limited by effective public health measures. Effective surveillance of travel-related infection informs provision of evidence-based health advice to the traveller2 and helps protect the domestic population from imported pathogens.
The risk of infection in travellers varies with destination, point of origin and type of travel.3,4 Travel-related illnesses are not limited to the exotic: travellers may encounter infections abroad which are also found at home, where the risk of exposure is different or reduced. Fever and acute diarrhoea are common5 and it has been noted that travellers to developing countries are often affected by gastrointestinal infections and by respiratory infections.6 Skin disorders are also commonly reported.7,8 Disease may also be observed in those arriving from permanent residence abroad, as exemplified by a proportion of imported malaria diagnosed in Scotland each year.9
Scotland, in common with the rest of the United Kingdom, has rigorous procedures for the management of those individuals diagnosed with infections of high consequence, including viral haemorrhagic fever.
In this report we summarise 1) recent travel trends as a context and 2) laboratory notifications of travel-related significance.
Travel abroad 2000 - 2015
Travel from the UK
Travel from the UK increased the start of the millennium until beginning to fall in 2008/2009, declining to 55.6 million journeys in 2010. Since that point, numbers have increased again to 65.7 million in 2015.10 Travel to North America from the UK has declined between 2000 and 2015, while travellers to Asia have increased in number since 2010. There has been a small decrease in travel to Africa since 2008 while travel to Latin America and the Caribbean has been steady. Travel to the Middle East has risen gradually since 2000.
Of 65.7 million foreign visits by UK residents in 2015, 79% were to Europe, with another 6%, 5%, 4%, 3% and 2% of journeys to North America, Asia, Africa, and Latin America & Caribbean and the Middle East respectively. Travel to Australia and New Zealand accounted for 1% of foreign visits. From 2010 to 2015, non-business travel increased annually by 3% while business travel has increased annually by 5%.
Travel from Scotland
In 2015, there were 4 million journeys abroad from Scotland, an increase of 3% from the previous year, representing 6% of total journeys from the UK. Europe (78%) was the most visited destination followed by North America (8%), Asia (4%), Africa (3%), Latin America and Caribbean (2%), the Middle East (2%) and Australia and New Zealand (1%). These proportions are similar to those recorded in 2014.
Surveillance of travel-related infections
Results of positive laboratory tests for a wide range of pathogens are received at Health Protection Scotland by electronic transfer through ECOSS.11 Clinical details are only received by ECOSS if they have been recorded in text accompanying the laboratory result. The data for 2016 for selected organisms were collated, episode criteria checked and duplicates removed.
HPS assumes infections such as schistosomiasis, vector-borne viruses, trypanosomiasis and leishmaniasis are always travel-related when they are identified in Scotland. Infections that can also be transmitted in the UK are only classified as imported when the appropriate information is recorded in the ECOSS report.
Escherichia coli O157, viral hepatitis and malaria figures for 2016 will be reported elsewhere.
All reports are subject to review and results presented here may be revised in future publications of this or other HPS reports. A total of 1443 episodes of travel-related infection are reported here, an increase of 15% from 2015 when there were 1250 episodes.
There were 231 episodes of Giardia in 2016, of which 42 (18%) were reported as imported. In 2015 there were 195 episodes, of which 39 (20%) were reported as imported. 785 episodes of Cryptosporidium in 2016 included 55 (7%) which were imported. The total for 2015 was 721, of which 60 (8%) were imported. Five episodes of Entamoeba histolytica were reported in 2016, all of which were imported. In 2015, there were three episodes of E. histolytica, again all imported. In 2016, 56 (34%) of 167 episodes of Cyclospora were recorded as imported. In 2015 there were 24 episodes of Cyclospora infection, of which eight (33%) were reported as imported.
Ten episodes of enteric fever were reported to HPS in 2016, of which three were Salmonella Paratyphi and seven were S. Typhi. Seven (70%) of these were imported. In 2015 there were nine reports of enteric fever, eight (89%) of which were imported.
Eighty-seven Shigella episodes were reported to HPS in 2015, compared to 110 episodes in 2013. Of those reported in 2016, there were 44 Shigella sonnei, 37 episodes of S. flexneri, three S. boydi and two S. dysenteriae. One episode of Shigella was unspeciated. Thirty-one percent of Shigella episodes were imported in 2016 compared to 35% in 2015.
Seven Vibrio episodes were reported in 2016, the same number as in 2015. The 2016 total comprised four Vibrio parahaemolyticus and three V. cholerae (non 01/0139). All Vibrio episodes in 2016 were imported, as was the case in 2015.
In 2016 there were four episodes of Rickettsia, comprising one Rickettsia prowazekii, two Rickettsia sp. (Spotted Fever group) and one Rickettsia sp. all of which were recorded as imported, compared to seven episodes of Rickettsia in 2015, all of which were also imported.
All vector-borne viruses reported in Scotland in 2016 were imported. There were 26 episodes of dengue virus in 2016, compared to 2015 when there were 30. The number of episodes of chikungunya virus rose to 16 in 2016 from four in 2015.
Zika virus totals for all of the United Kingdom are reported by Public Health England.12
Four episodes of Leishmania were reported in 2016. Of these, one was Leishmania viannia, one was L. braziliensis, one L. mexicana and one Leishmania sp. In 2015, there were three episodes of Leishmania: one L. viannia, one L. braziliensis and one unspeciated. It is assumed all Leishmania infections are imported.
One hundred and one episodes of Schistosoma infection were reported in 2016. In 2015 there were 133 episodes. It is assumed all Schistosoma infections are imported.
Surveillance and significance of results
As in previous years, this report considers only those infections where a specimen was tested or examined. It is likely that most investigations are predicated on reported symptoms, but it is also possible that some positive results are related to patients who were tested on a precautionary basis. Positive results alone do not indicate the extent to which the patient was unwell and in some cases with potential for serious outcomes e.g. Zika virus disease symptoms may be trivial.
HPS receives no information on those infections that are acquired abroad but resolve before arrival in Scotland. Thus, taken in isolation, ECOSS data cannot accurately estimate total levels of disease in the travelling population. Clinical and travel histories are often absent from laboratory reports and in all circumstances, surveillance benefits from effective communication between epidemiologists and physicians. The number of imported infections is likely to be underestimated as the appropriate information is recorded inconsistently in ECOSS. This is probably the case in many or most of the Cyclospora infections reported here.
For some pathogens e.g. flaviviruses,13,14,15 a positive test result may arise from vaccination or cross-reaction. Positive yellow fever IgG results are seen frequently, but unless followed by a rising IgG titre or accompanied by a positive IgM or PCR result they are usually discounted.
In 2016 testing for Zika virus presented challenges for UK public health agencies: validated assays were initially unavailable and PCR also presented challenges, as viraemia in Zika virus infection is usually short-lived. All Zika virus testing was performed at Public Health England’s Rare & Imported Pathogens Laboratory (RIPL).16
Organisms such as Salmonella, Shigella, Giardia and Cryptosporidium causing traveller’s diarrhoea (TD)17,18 remain the most commonly reported infections. As in previous years, a small number of infections caused by Vibrio species were identified in Scotland in 2016. An outbreak of cyclosporiasis in Europe and North America began in 2015 with travel to Mexico associated with some cases.
In 2016, HPS worked with microbiologists, health protection teams and colleagues in Public Health England (PHE) and the other devolved administrations to investigate a large outbreak of Cyclospora among travellers returning to the UK from Mexico with the majority of cases reported in July and August.19 This was the second consecutive year that an outbreak of Cyclospora among travellers returning from Mexico had been identified in the UK, with a smaller outbreak in 2015.20
Cyclospora most often occurs in tropical and subtropical regions of the world including South and Central America, South and South East Asia, the Middle East and Africa, information on Cyclospora for those travelling to these regions is available at https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/545769/Cyclospora_advice_sheet.pdf.
Once again, dengue virus was the most frequently-reported vector-borne virus in Scotland, although the number of episodes reported in Scotland fell in 2016, while episodes of chikungunya rose in number.
Dengue and chikungunya viruses occur across the tropics and subtropics and are increasingly found in warmer areas of the temperate zone, with transmission occurring in Italy (chikungunya)21 and metropolitan France (dengue)22 in recent years. Chikungunya and dengue are unrelated to each other but can be transmitted by the same Aedes sp mosquito vectors23 so may occur together. Major outbreaks of dengue and chikungunya have been ongoing in the Caribbean and the Americas for the past three years24,25 with Asia and the Pacific region also experiencing a significant burden of disease.26 In some countries one or both of these viruses has replaced malaria as the most significant vector-borne infection. Vector-borne viruses may present a greater challenge to the traveller than does malaria. Bite avoidance is the only preventive measure for most and this may prove insufficient in countries with high mosquito density and high viral incidence in humans or other mammals.
Zika virus, a flavivirus transmitted by Aedes mosquitoes, has spread across a range similar to that of dengue and chikungunya in the past three years. Notably, it has spread rapidly through Brazil and neighbouring countries and has been identified as the cause of an increased incidence of developmental defects including microcephaly in newborns.27,28 The birth defects seen in Brazil do not appear to have occurred with similar frequency elsewhere, even in those countries where Zika virus disease has been widespread. An outbreak of Zika virus disease in Florida gave cause for concern in the UK, as Florida is a popular destination for travellers from the UK. Zika virus is not a new infection in humans and it is increasingly apparent that it has been circulating in Africa for longer than previously recognised. Being a relatively mild febrile illness that is hard to diagnose clinically, Zika virus disease is difficult to monitor in a continent where febrile illness of varying severity is widespread.
Zika virus disease is generally a mild illness characterised by non-specific viral symptoms.29 It has a similar clinical presentation to dengue, but symptoms are usually less severe. There is no vaccine and no specific treatment is indicated. However, pregnant women who have had Zika virus disease require counselling and monitoring, such are the concerns about the effects of the virus on the developing fetus.
Many vector-borne viral infections share a clinical picture of fever, nausea, joint pain, myalgia and rash. Overlapping geographic ranges of viruses adds to the difficulty of differential diagnosis. Although a dengue vaccine has now been approved in Mexico, the Philippines, Brazil, El Salvador, Costa Rica, Paraguay, Guatemala, Peru, Indonesia, Thailand and Singapore,30 the most important method of preventing most mosquito-borne viral infections is rigorous bite avoidance.31 In this regard, prevention of Zika virus with its uncertain consequences is the same as for other potentially serious mosquito-borne viruses where no vaccine is available.
Of the mosquito-borne viruses, yellow fever is the best known and often considered to have the most dangerous epidemic potential. In 2016 there were outbreaks in several African countries and late in the year Brazil also began to see cases as the current outbreak began in that country. Yellow fever vaccine is effective but expensive and there has been a shortage of production in recent years. Vaccination is mandatory for entry to many countries, but despite this there has been an increase in yellow fever imported into Europe in the past year.32 Despite the presence of mosquitoes with potential to transmit yellow fever, the risk of transmission in Europe is considered to be low. The outbreaks in Africa and South America have not, as yet, led to the importation of yellow fever into the United Kingdom, but the risk of travellers’ exposure is likely to increase.
The number of Schistosoma episodes reported in Scotland has fallen in 2016. In the main, schistosomiasis affects travellers exposed in historically endemic areas, although Schistosoma haematobium was identified in European travellers returning from Corsica in 2014.33 Visits to Africa by Scottish school students are frequent and may increase the risk of exposure to schistosomes and other infectious organisms.34 All schools planning travel abroad are encouraged to seek appropriate guidance well in advance of departure.35
Schistosoma burdens are usually low in travellers with infrequent or brief exposure, meaning symptoms are usually absent or trivial. Few reports of schistosomiasis are indentified to species level as diagnosis is by serology in nearly all cases.36 Health Protection Scotland and the Scottish Parasite Reference Laboratory are collaborating in order to carry out enhanced surveillance of schistosomiasis imported into Scotland in 2017 in order to improve how guidance is delivered. Information on where travellers from Scotland become infected with Schistosoma sp has previously been incomplete to date.37
Food and water hygiene remain essential methods for protecting the health of the travelling public, as gastrointestinal infections are again the most commonly reported. Vaccination is also an important method of prevention for some food and water-borne diseases i.e. hepatitis A, typhoid, cholera and poliomyelitis.
Vector-borne infections were more frequently reported than in 2015 and this continues to highlight the need for rigorous bite avoidance and vaccination where possible and appropriate. Clinicians advising travellers to Zika virus-affected areas should consult current Health Protection Scotland guidance.1 The possibility that Zika virus may have serious consequences for the developing fetus means that pregnant women should exercise caution when considering travel to areas where Zika virus is present. If travel is unavoidable, pregnant women should be especially conscientious in avoiding mosquito bites at all times. Indeed, bite avoidance by all travellers will help reduce the risk of becoming infected by any mosquito-borne infection.
Any returning traveller who becomes unwell should seek medical advice and report their travel history to their health care provider. HPS encourages all clinicians requesting laboratory testing for infectious disease to take a full travel history, and to provide this information on the laboratory request form.
It is important to diagnose and treat infectious disease in newly-arrived travellers promptly and appropriately and in so doing seek both to improve the patient’s condition and to preserve public health. In this regard, the health of travellers and the health of resident populations are not considered to be entirely separate issues. In the context of migration, health professionals seeing new arrivals presenting with infectious disease are encouraged to liaise appropriately with laboratory staff, infectious disease clinicians and health protection teams where necessary.
Up-to-date, expert advice on travel health and country-by-country disease risks is available to healthcare professionals on TRAVAX (http://www.travax.nhs.uk). Travellers are strongly advised to consult the fitfortravel website (http://www.fitfortravel.nhs.uk) in advance of their journey for information on how to stay healthy abroad. The website includes country-specific advice on recommended vaccines and antimalarial chemoprophylaxis, and details on safe food and water, accident avoidance, sun protection and insect bite avoidance. TRAVAX recommends that travellers consult a GP, practice nurse or travel health clinic at least six weeks before travel.38
- Health Protection Scotland. Zika Virus information and guidance. Available from: http://www.hps.scot.nhs.uk/internationalissues/zika.aspx. (accessed 25 April 2017).
- Fitfortravel. Travel health advice. 2017. Available from: http://www.fitfortravel.nhs.uk/advice.aspx. (accessed 25 April 2017).
- Heywood AE, Forssman BL Seale H et al. General practitioners’ perception of risk for travelers visiting friends and relatives. Journal of Travel Medicine. 2015;22(6):368-374. Available from: http://onlinelibrary.wiley.com/doi/10.1111/jtm.12229/full. (accessed 25 April 2017).
- Shlim DR. Perspectives: travelers’ perception of risk. In: CDC Health Information for International Travel (2016 Yellow Book). Available from: https://wwwnc.cdc.gov/travel/yellowbook/2016/the-pre-travel-consultation/perspectives-travelers-perception-of-risk. (accessed 25 April 2017).
- Munro J, Redman C, Smith C et al. A report on GeoSentinel data collected at the Brownlee Centre for Infectious & Communicable Diseases, April 2011 - March 2013. HPS Weekly Report. 2014; 48 (2014/44): 571-582. Available from: http://www.hps.scot.nhs.uk/ewr/redirect.aspx?id=61343. (accessed 25 April 2-17).
- Redman CA, MacLennan A, Wilson E et al. Diarrhea and respiratory symptoms among travelers to Asia, Africa and South & Central America from Scotland. Journal of Travel Medicine. 2006;13:203-211. Available from: https://academic.oup.com/jtm/article-lookup/doi/10.1111/j.1708-8305.2006.00046.x. (accessed 25 April 2017).
- Freedman DO, Weld LH, Kozarsky PE et al. Spectrum of disease and relation to place of exposure among ill returned travelers. New England Journal of Medicine. 2006;354:119-130. Available from: http://www.nejm.org/doi/full/10.1056/NEJMoa051331#t=article. (accessed 25 April 2017).
- Gautret P, Schlagenhauf P, Gaudart J et al. Multicenter EuroTravNet/GeoSentinel study of travel-related infectious diseases in Europe. Emerging Infectious Diseases. 2009;15(11):1783-1790. Available from: https://wwwnc.cdc.gov/eid/article/15/11/09-1147. (accessed 25 April)
- Munro J, Smith V, Smith C, Redman C. Travel health: Malaria in Scotland and the UK: 2009-2013. HPS Weekly Report. 2014;49(2015/30):279-292. Available from: http://www.hps.scot.nhs.uk/ewr/redirect.aspx?id=59738. (accessed 25 April 2017).
- Office for National Statistics. Data and commentary from Travel Trends, 2015. Available from: https://www.ons.gov.uk/peoplepopulationandcommunity/leisureandtourism/articles/traveltrends/2015. (accessed 25 April 2017).
- Health Protection Scotland. Electronic communication of surveillance in Scotland (ECOSS). Available from: http://www.hps.scot.nhs.uk/surveillance/SystemsDetail.aspx?id=248. (accessed 25 April 2017).
- Public Health England. Zika virus (ZIKV): clinical and travel guidance. Available from: https://www.gov.uk/government/collections/zika-virus-zikv-clinical-and-travel-guidance#epidemiology-and-cases-diagnosed-in-the-uk. (accessed 28 April 2017).
- Koraka P, Zeller H, Niedrig M et al. Reactivity of serum samples from patients with a flavivirus infection measured by immunofluorescence assay and ELISA. Microbes and Infection. 2002;4(12):1209-1215. Available from: http://www.sciencedirect.com/science/article/pii/S1286457902016477. (accessed 25 April 2017).
- Peeling RW, Artsob H, Pelegrino JL et al. Evaluation of diagnostic tests: dengue. Nature Reviews Microbiology 2010; December: S30-S37. Available from: http://www.nature.com/nrmicro/journal/v8/n12_supp/full/nrmicro2459.html. (accessed 25 April 2017).
- Mansfield KL, Horton DL, Johnson N et al. Flavivirus-induced antibody cross-reactivity. Journal of General Virology. 2011;92(12):2821-2829. Available from: http://jgv.microbiologyresearch.org/content/journal/jgv/10.1099/vir.0.031641-0. (accessed 25 April 2017).
- Public Health England Rare and Imported Pathogens Laboratory (RIPL). Available from: https://www.gov.uk/government/collections/rare-and-imported-pathogens-laboratory-ripl. (accessed 25 April 2017).
- Hill DR. Management of travellers’ diarrhoea. British Medical Journal 2008;337:a1746. Available from: http://www.bmj.com/content/337/bmj.a1746. (accessed 25 April 2017).
- Gautret P, Cramer JP, Field V et al. Infectious diseases among travellers and migrants in Europe, EuroTravNet 2010. Eurosurveillance. 2012;17(26):16-26. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20205. (accessed 25 April 2017).
- HPS. Cyclospora update - advice for travellers HPS Weekly Report. 2016; 50 (2016/33): 254-255. Available from: http://www.hps.scot.nhs.uk/ewr/redirect.aspx?id=69127. (accessed 25 April 2017).
- Nichols GL, Freedman J, Pollock KG et al. Cyclospora infection linked to travel to Mexico, June to September 2015. Eurosurveillance. 2015;20(43):2-5. Available from: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=21284. (accessed 25 April 2017)
- Rezza G, Nicoletti L, Angelini R et al. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet. 2007;370(9602):1840-6. Available from: http://www.thelancet.com/journals/lancet/article/PIIS0140-6736(07)61779-6/fulltext. (accessed 25 April 2017).
- European Centre for Disease Prevention and Control. Communicable disease threats report, 20-26 September 2015, week 39. Available from: http://ecdc.europa.eu/en/publications/Publications/communicable-disease-threats-report-26-sep-2015.pdf. (accessed 25 April 2017).
- Kraemer MUG , Sinka ME, Duda KA et al. The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife. 2015;4:e08347. Available from: https://elifesciences.org/content/4/e08347. (accessed 25 April 2017).
- PAHO/WHO. Annual Cases Reported of Dengue. Available from: http://www2.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=6290&Itemid=40734&lang=en. (accessed 25 April 2017).
- PAHO/WHO. Chikungunya in the Americas. Available from: http://www2.paho.org/hq/index.php?option=com_topics&view=rdmore&cid=8975&Itemid=40931&lang=en. (accessed 25 April 2017).
- WHO/WPRO. Dengue situation updates. Available from: http://www.wpro.who.int/emerging_diseases/DengueSituationUpdates/en/. (accessed 25 April 2017).
- PAHO/WHO. Regional Zika Epidemiological Update (Americas) March 10, 2017. Available from: http://www2.paho.org/hq/index.php?option=com_docman&task=doc_view&Itemid=270&gid=38610&lang=en. (accessed 25 April 2017).
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