Insect-borne diseases

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Insect-borne diseases

Insect-borne diseases impose immense health and economic burdens on both individuals and nations. Millions of people are affected directly by infections that cause debilitation, disfigurement, disabilities such as blindness.

On the national scale, healthcare systems can be overwhelmed and suffer significant loss of productivity caused by the numbers unable to work efficiently. Companies that trade in products that require a high degree of hygiene and cleanliness, such as food and pharmaceuticals, can suffer economic and reputational loss by contamination from insects.

With concerted action by the international community, some diseases endemic in developing countries have been drastically reduced. The number of cases of human African trypanosomiasis has reduced by 90%, and lymphatic filariasis may be eliminated in six countries, according to WHO (2015), which is studying these areas for verification. There is also concerted action to eliminate other major diseases that affect millions, such as malaria and Chagas disease.

Complacency, however, has resulted in several insect-borne diseases being almost eliminated then returning with a vengeance. Following the development and widespread use of insecticides in the middle of the 20th century several diseases were targeted in control programmes that had great success. When the threats were reduced, programmes were terminated, expertise was lost, and infrastructure disappeared. Diseases returned to epidemic proportions and required multi-agency collaboration in the international community to restart control programmes. This shows that continuous monitoring and maintenance of skills in healthcare, entomology, vector control, etc, are essential.

With rapid climate and man-made environmental changes new diseases are also becoming more prominent. Dengue fever cases, for example, have multiplied 30 times over five decades as urbanisation has spread in developing countries. Some diseases are being seen in places previously separated from the vectors by physical and climatic boundaries as vectors that are carried around the world through trade, migration and travel, gain a foothold in new locations.

The Tiger Mosquito, Aedes albopictus, for example, is a prolific breeder in man-made environments and a vector for several diseases including dengue, West Nile fever and Japanese encephalitis. It has spread well outside its natural range in south and east Asia. It is now present in North and South America, Africa, Australia and southern regions of Europe, since being spread by trade in used tyres. It is classed as one of the World’s Worst Invasive Alien Species by the IUCN. In 2015 Austria reported its first case of West Nile fever, and it was also reported in Italy, Bulgaria and Romania, Israel and Serbia. It is one of several vector species being monitored by the VectorNet project of the European Centre for Disease Prevention and Control.

The impact of many damaging diseases in the tropics and developing countries is well known, but a number of diseases already have significant impact in the developed world and others are growing in importance due to climate change. Asthma, for example, which is an allergic reaction to a range of microscopic particles, including from the house dust mite and cockroaches, was estimated by WHO in 2006 to affect 300 million people worldwide. In the US and some other countries it is the leading cause of hospital visits for children. Insect borne diseases, therefore, have a major impact on the people, health services and economies of both developed and developing countries.

Disease transmission

Insect borne diseases can be transmitted actively or passively in two ways:

  • biologically: the disease-causing organism is carried within the animal body where it multiplies, breeds or passes through a phase of its life cycle, before being delivered into a new host, usually by biting to feed on blood. In a few cases the organism is released by the arthropod defecating on the person’s skin or through the squashed bodies and rubbed into a bite or wound, or passed into the mouth, eyes or nose by dirty hands.
  • mechanically: flies, cockroaches and beetles pick up the disease causing organisms by physical contact with filth, waste and contaminated materials, or feeding on it. The organism is then transmitted passively by faecal deposition, regurgitation, or carrying it on the outside of their bodies to surfaces and food products in the human environment.

Cockroaches and house flies, which are common around the human environment, do not bite but can be mechanical carriers of a large variety of pathogenic bacteria, fungi (inc. moulds), helminths, protozoans and viruses. In developing countries especially they can be present in large numbers in hospitals, food stores, houses, animal sheds and restaurants, and are major vectors of diarrhoea and dysentery-causing organisms such as Salmonella and Shigella species, including drug-resistant strains.

Chagas disease

Insect: Assassin Bugs/ Kissing bugs/ Triatomine bug
Organism: protozoan: Trypanosoma cruzi

Chagas disease is also referred to as American trypanosomiasis. There are 150 species of the bug and more than 100 species of mammal carry the protozoan parasite. It is classified by WHO as a neglected tropical disease, with 8 million people infected, mainly in central and South America, and an estimated 10,000 deaths caused by complications from the disease.

Both the adults and nymphs, male and female, are blood-feeders and so search for human hosts to feed on, especially exposed areas such as the face. However, they carry the parasite in their faeces which is deposited onto the skin after feeding. When a person inadvertently wipes their contaminated skin this can carry the protozoan into the bite, other broken skin, or the eyes and mouth. It can also be spread through blood transfusion, organ transplantation, and eating food contaminated with the parasites.

Symptoms generally start off as mild fever, swollen lymph nodes, headaches, local swelling at the site of the bite, then may disappear. However, 30 to 40% of people develop further symptoms 10 to 30 years after the initial infection, including enlargement of the ventricles of the heart, heart failure, enlarged esophagus or enlarged colon.

Dengue

Insects: Mosquitoes
Organism: Dengue virus

Dengue is the most important mosquito-borne viral disease in the world, according to WHO, which has targeted it as one of 17 Neglected Tropical Diseases for major campaigns for awareness and eradication. It is endemic in over 100 countries across the tropics, from central and South America, Africa, South and Southeast Asia and to the Pacific Islands. It has increased rapidly over the last few decades in urban sprawls that provide ideal conditions for breeding. The WHO estimates that there are 50-100 million infections a year and half the world’s population live in countries where it is endemic.

The threat of Dengue is greater than the current outbreaks as the mosquito vectors are present in a far wider geographic range, and the Tiger Mosquito Aedes albopictus, especially is widening its range. New cases were reported in Croatia, France, Madeira Islands, Florida (USA) and Yunnan (China) in the last few years.

The majority of cases have no symptoms or mild fever, while about 5% have severe illness that shows as sudden fever 3-14 days after infection, with headache, muscle pain, joint pain, and a body rash. There is no vaccine and no specific treatment.

Malaria

Insect: mosquitoes
Organism: protozoan, Plasmodium falciparum, P. vivax, P. ovale, P. malariae, P. knowlesi

Malaria causes up to a million deaths a year and is estimated to infect over 200 million people worldwide. It is present in 97 countries covering half the world’s population. Around 90% of deaths occur in sub-Saharan Africa, especially Nigeria and the Democratic Republic of the Congo. Those most at risk are the poor in remote communities with few health facilities, the young, pregnant women and people with HIV.

The parasite has a complex life cycle, having a series of stages in the mosquito and the animal host. In the host, one form can live in the liver for up to 30 years producing no symptoms; other forms grow and reproduce in the red blood cells, including male and female forms that can infect mosquitoes.

The symptoms of fever, headache and vomiting show 7-15 days after infection. If not treated, P. falciparum can multiply rapidly and block small blood vessels in vital organs including in the brain. Other types have dormant liver stages that can reactivate months or years later.

West Nile Fever

Insect: Mosquito.
Organism: Flavivirus, West Nile virus.

The disease was virtually unknown outside Uganda, where it was first identified in 1937, until the 1990s, when there was an outbreak in Algeria. It is now present in all temperate and tropical continents, with even the US experiencing an outbreak in 2012 that killed 286 people. The European Centre for Disease Prevention and Control monitors infections in Europe and in 2015 reported eight human cases of WNF in EU Member States up to August: Austria (1), Italy (4), Bulgaria (1), Romania (1) and Austria (1). Eight cases were detected in neighbouring countries: Israel (7) and Serbia (1). It even produces an interactive map of cases.

Around 80% of people infected do not show any symptoms. In the remainder, symptoms appear in 2-15 days, including fever, headache, body aches, joint pains, vomiting, diarrhoea or rash. Most people recover completely, but weakness can last for weeks or months. A small number of patients develop encephalitis, meningitis or poliomyelitis. There is no specific treatment and no vaccine.

Yellow fever

Insects: Mosquitoes
Organism: Virus, Flavivirus

Yellow fever is a haemorrhagic fever that originated in the central belt of Africa but spread to South America in the 17th century with the slave trade. It is endemic in 34 countries in Africa where the majority of the estimated 30,000 deaths from 200,000 infections a year occur. It has three patterns of transmission:

  • urban, transmitted by A aegypti, which breeds in fresh water in the human environment such as tin cans, water drums, gutters, etc. This is the main mode of infection in Africa;
  • forest pattern, transmitted by mainly A. africanus, A. bromeliae, where monkeys are the primary host. This is the main pattern in South America; and
  • an intermediate or ‘savannah’ pattern, which has become more prominent in Africa recently.

Symptoms show 3-6 days after infection, including fever, headache, backache, general muscle pain, nausea, and vomiting. About 15% of cases develop into an acute, toxic phase with jaundice due to liver damage and haemorrhagic signs — bleeding in the mouth, eyes, nose, and gastrointestinal tract giving ‘black vomit’. This stage is fatal for 20% or more of patients.

A safe vaccine is available and gives protection for at least 10 years.

Asthma

Insect: House dust mites & Cockroaches.
Organism: none known (allergic response).

Asthma is not caused by an infectious organism but by an allergic reaction to particles shed by organisms, mainly house dust mites and cockroaches. So it does not strictly come under vector-borne disease.

It is, however, of great significance to the health and economies of developed countries. It is one of the most common chronic diseases of children and in the US is the leading cause of hospital admissions for children. The WHO estimates that 300m people have asthma worldwide, ranging from 1% in rural Africa to 7-20% in Europe and 25-40% in some cities of the US and Australia.

The main cause is house dust mites, which are arachnids less than one millimetre long that feed mainly on human skin scales. Pollen, spores of microorganisms, fungal mycelia and bacteria have also been found in the gut of house dust mites. They live in the small spaces provided by mattresses, carpets, duvets, pillows and furniture materials, whether natural or synthetic, as both provide ideal shelter.

The mites depend on a suitable relative humidity and temperature for survival, so heating, ventilation and moisture control in places that they inhabit affects their numbers. Optimal conditions are 25°C and 75% relative humidity, which allows development from egg to adult in about 25 days. D. farina can survive low humidity conditions by forming a ‘protonymph’ stage that is drought resistant. It is the most common species in regions with prolonged dry weather such as the US. In areas with higher humidity D. pteronyssinus and E. maynei are the most common.

The German cockroach is the main cockroach pest species, inhabiting human buildings on all continents except Antarctica, but needing the building (or ship) environment to survive in cold climates. It occurs especially in restaurants, hotels, hospitals, nursing homes and food processing facilities. Many studies have shown that exposure to cockroach allergens is associated with asthma. In some studies in the US a high proportion of asthmatics had cockroach sensitivity, especially in urban areas, showing the prevalence of the pest even in the US.

African Trypanosomiasis

Insect: Tsetse fly, horse fly, Tabanidae
Organism: protozoa, Trypanosoma brucei subspecies gambiense and rhodesiense

Also referred to as sleeping sickness, this disease is only found in rural Africa, affecting mainly poor rural communities. It was brought under control in the 1960s but re-emerged in the 1970s as control measures were relaxed. The rates of infection have dropped drastically in the last 20 years from an estimated 300,000 to under 30,000, according to WHO, as a result of disease-control campaigns. In May 2015 WHO reported that the number of cases had dropped to 3800, its lowest level in 75 years. Control efforts still screen 2-3 million people a year in local health centres.

The tsetse fly lives in woodland, forest and vegetation. Both male and female feed on blood and seek a meal during daylight hours. Domestic and wild animal reservoirs play a major role in transmission of the disease.

There are two subspecies of the parasite that are found in different areas of Africa — East African sleeping sickness and West African sleeping sickness. Once in a human host, the protozoan first circulates and multiplies in the blood and lymph system, producing symptoms of fever, swollen lymph nodes and skin itching. It can then invade the brain and central nervous system, which causes headaches, drowsiness, and abnormal behaviour. It can lead to coma and death if not treated.

Amoebic dysentery

Insects: cockroaches, flies
Organism: protozoan, Entamoeba histolytica

Insects are vectors of amoebic dysentery by mechanical transmission of the protozoa from direct contact with human faeces or contaminated products and surfaces. It is estimated that 50 million people are infected worldwide, but the majority of cases are asymptomatic, with only 10% showing disease symptoms.

The disease causes bloody diarrhoea, weight loss, fatigue and abdominal pain. The organism can invade the intestinal wall, producing ulceration. It can then pass into the blood stream and enter other organs, particularly the liver.

Anthrax

Insect: horse fly, deer fly, house fly, blow fly, mosquitoes.
Organism: bacteria, Bacillus anthrax.

Many types of biting and non-biting insects have been incriminated in spreading anthrax during outbreaks and also shown to spread it in controlled conditions. This can occur directly by carrying the bacteria from one animal to another or by feeding on carcasses then depositing faeces or vomit on plants that are then browsed by grazing animals. The dormant spore phase of anthrax can last for decades in soil, until ingested or inhaled by grazing animals, and then activated by the suitable conditions in the host.

Human infection has three routes of entry:

  • pulmonary — inhalation of spores mainly from infected animal hides and other animal products. Symptoms start as flu-like then pneumonia and respiratory collapse over several days. With treatment, fatality rates are around 45% (in the 2001 anthrax attacks in the US when spores were sent by post).
  • gastrointestinal — consumption of infected meat, causing severe diarrhoea, acute inflammation of the intestinal tract, vomiting of blood. Fatality rates are 25-60%.
  • cutaneous — spores enter through cuts in the skin when handling infected animals or animal products, causing skin ulcers. Without treatment fatality rates are about 20%.

Bartonellosis

Insect: fleas, body louse, sand flies, ticks, mosquitoes.
Organism: bacteria, Bartonella spp

Bartonella species of bacteria are responsible for a number of diseases including:

Trench fever
Caused by B. Quintana, the disease is spread by the human body louse. It is notorious for affecting large numbers of troops during the First World War — over one-fifth of British, German and Austrian troops reporting ill had trench fever. It is present around the world, with cases reported in Europe, North America, Africa and China. Symptoms include fever, headache, rash, and bone pain, mainly in the shins, neck, and back.

Cat-scratch disease
This is caused by several Bartonella species and as its name suggests it can be transmitted by a scratch from a cat that has been infected by cat fleas carrying the bacteria. It is most common in kittens and children. Symptoms include heart inflammation (endocarditis, myocarditis) and eye disease (neuroretinitis). It is also thought to be spread by flea or tick bites.

Carrión's disease
Confined to higher elevations in western South America, it is spread by Lutzomyia sandfly bites. It produces two distinct phases, a fever termed Oroya fever (originally thought to be a separate disease), and skin lesions that tend to bleed. It is named after a Peruvian medical student who infected himself with the disease in 1885 to record its progression and died as a result.

Chikunguya fever

Insect: mosquitoes
Organism: virus, Chikunguya virus.

Chikunguya fever occurs across a broad band of the tropics from the Atlantic coast of Africa to Papua New Guinea in the western Pacific. Cases have also been reported in South and Central America, US, southern Europe.

The main symptoms are fever, severe joint pain for several weeks, skin rash, muscle pain, headache, nausea, fatigue. Most patients recover but the joint pain may last for months or years. There is no vaccine or specific treatment. It is similar to Dengue fever for the vectors, symptoms, apart from joint pain, and geographical area.

Cholera

Insect: House Fly, Blow Fly, Flesh Fly
Organism: bacteria, Vibrio cholera.

Cholera is a disease of poor sanitation, poverty and conflict, caused by ingestion of faecally contaminated food and water. Insects play a role in spreading the disease by carrying the bacteria from infected faeces and contaminated products around the human environment.

The incubation period is one to five days, after which the bacteria produces a toxin that causes large amounts of watery diarrhoea and vomiting leading to severe dehydration and death if not treated — 25-50% of severe cases are fatal.

A vaccine is now available and has been used successfully by WHO to control outbreaks in recent years, with 2 million doses distributed since 2013, mainly in areas of conflict in Africa. Africa generally accounts for over 90% of cases, with the exception of the outbreak in Haiti and neighbouring countries following the 2010 earthquake, when the global cases peaked at almost 600,000 in 2011.

According to WHO, 80% of cholera cases can be treated using only oral rehydration salts, yet 748 million people lacked clean water in 2012 and 45 countries were lagging behind in improving water supplies.

Epidemic typhus

Insect: Louse.
Organism: bacteria, Rickettsia prowazekii

As with other louse-borne fevers, typhus tends to occur in conditions of overcrowding and poor hygiene such as refugee camps and prisons. It occurs mainly in central and eastern Africa, central and South America, and Asia. Recent outbreaks have occurred in Burundi, Ethiopia and Rwanda. Infection occurs from crushing the lice or rubbing the skin where the lice are feeding and defecating and carrying the bacteria to wounds and mucous membranes. Some cases in the US have been associated with flying squirrels nesting in houses over winter, but the means of infection is still unknown as the patients did not have lice.

The symptoms can include high fever, headache, severe muscular pain and after 5-6 days a rash of dark spots.

Japanese encephalitis

Insect: mosquito
Organism: flavivirus, Japanese encephalitis virus.

Japanese encephalitis occurs mainly in rural areas of East, Southeast and South Asia. Infection rates are associated with the rainy season and flooding of paddy fields. The main hosts of the virus are pigs and wading birds, with humans as incidental hosts that rarely pass on the disease through further bites. It is closely related to West Nile virus and St. Louis encephalitis virus.

The majority of infections do not show any symptoms, but in a few cases, especially children, the virus invades the brain and high fever symptoms and headache start showing after 5-15 days. This develops into coma, tremors and convulsions. There is no specific treatment but vaccines are available.

Leishmaniasis

Insect: Sandflies
Organism: protozoa, Leishmania spp

Leishmaniasis is spread by bites from female sandflies. These are tiny flies 1.5-3.0 mm long with large black eyes and hairy bodies, wings and legs. They breed in forest areas, caves and adobe brick houses where most of the infection of humans takes place. Rodents, dogs and other mammals are reservoirs for the disease.

There are more than 20 species of the protozoan that produce several forms of the disease: cutaneous, mucosal and visceral, causing variously, skin sores, chronic ulcers, mucosal infections, and infections of the spleen, liver, bone marrow and lymph nodes. The disease occurs in many countries in tropical and subtropical regions, with the different forms more prevalent in certain countries, although Brazil is a major source of all three forms.

WHO has estimated that 310 million people are at risk from the disease. There are 300,000 cases of visceral leishmaniasis and over 20,000 deaths a year, while 1 million cases of the cutaneous form were reported over a five-year period (to 2012).

The bite leaves a non-swollen red ring and symptoms of infection are fever and anaemia.

Lymphatic filariasis

Insect: Mosquitoes
Organism: roundworm, Wuchereria bancrofti (90%), Brugia malayi, B. timori

The adult parasitic worm only lives in the human lymph system and is spread between people by mosquito bites. It affects more than 120 million people, according to WHO, of whom 40 million are disfigured or incapacitated, including 25 million men with genital disease. This results in large numbers of people suffering long term pain, loss of productivity — for their families and the economy — and social exclusion.

The worms can be present in the body for years without showing symptoms, slowly damaging the lymphatic system, kidneys and immune system as they produce millions of larvae over a lifetime of 6-8 years. The worst symptoms usually show in adults, more commonly men, producing inflammation of tissue (elephantiasis) in arms, legs, genitals and the lymphatic system (lymphedema).

Drugs are available that will clear the parasites from the bloodstream, so the disease can be eliminated with a concerted campaign.

Onchocerciasis/ River blindness

Insect: Blackfly
Organism: nematode worm, Onchocerca volvulus

River blindness affects 37 million people, mainly in 31 countries in Africa and also Central and South America. It is only a risk in remote rural areas near fast flowing streams where the blackfly breeds.

The parasite causes itching of the skin, lymphadenitis (hanging groins), elephantiasis of the genitals, serious visual impairment, and blindness.

The parasite has a complex lifecycle, only reproducing in humans and having several larval stages in the blackfly. The female blackflies seek a blood meal after mating and if they feed on an infected human can ingest the microfilariae stage from the blood. The microfilariae produce larvae, which have three stages, the last of which migrates to the head and proboscis of the fly and can infect humans via the saliva on biting.

The larvae migrate to subcutaneous tissue where they form nodules and mature into adults in 6-10 months. The adults mate and the female produces a microfilaria stage, which can then be ingested by the blackfly on feeding.

The adult nematode worm can grow to 50cm and live in the nodules for 15 years, producing the microfilaria stage for up to nine years.

Treatment is available to kill the microfilariae and relieve the skin itching, but not to kill the adult worms. However a potential new treatment has been reported by CDC using an antibiotic that kills a symbiotic bacterium, Wolbachia, that is essential for the parasite’s survival.

Pappataci fever

Insect: Sandfly
Organism: virus, Phlebovirus serotypes

There are three serotypes of the virus: Toscana, Sicilian and Naples. It occurs in a band around the Mediterranean, across the Middle East to northern India and southwest China. Symptoms appear a few days after infection: fever, severe frontal headache and muscle and joint ache, rapid heart rate and facial flushing, subsiding after two days. It is also known as three-day fever, phlebotomus fever and sandfly fever. There is no specific treatment.

Salmonellosis

Insect: house flies, blow flies, flesh flies, cockroaches
Organism: bacteria, Salmonella enterica

Salmonella bacteria can be carried by flies and cockroaches that inhabit ‘filth’ by mechanical transmission after contact with infected faeces from humans or animals and contaminated products.

In the US alone it is estimated to cause one million infections, 19,000 hospitalisations and nearly 400 deaths a year, according to CDC.

The Salmonella species of bacteria has a complex classification, having six subspecies which are further classified into 2500 serovars, a few of which are important causes of disease in humans.

Salmonellosis is caught mainly from contaminated water, foods, especially raw poultry, minced beef, and raw eggs. Poor hygiene in vegetable and fruit harvesting, and pets, especially reptiles, baby chicks and ducklings are also sources of infection. Avoidance of contact, general hygiene and hand hygiene are the most important means of prevention.

Symptoms include diarrhoea, fever, vomiting, and abdominal cramps. Most people recover in a few days without treatment other than replacement of fluid lost by the body. Once a person is infected however, the disease is easily transmitted to other people through poor hand hygiene and poor sanitation.

Typhoid fever
One serovar of Salmonella (Salmonella enterica subsp. enterica serovar Typhi) causes more severe infection and spreads from the intestines to the blood and lymphatic system and then to other body sites. It is endemic in many developing countries, where it affects around 27 million people a year, especially in India and in children. It only occurs in humans and is spread through faecal contamination, therefore poor hygiene plays a major role in maintaining its presence. It is treatable with antibiotics and a vaccine is available.

Shigellosis

Vector: House flies, blow flies, and flesh flies, cockroaches.
Organism: bacteria, Shigella species

Shigellosis is one of the major diarrhoea and dysentery causing organisms worldwide, responsible for about 90 million infections annually. It is caught by ingesting food and water contaminated with faeces from infected people. The bacteria only occurs in humans and primates so is dependent on poor hygiene for maintaining infections — only 10-100 bacteria are required to cause an infection.

Symptoms take up to a week to appear. The infection causes diarrhoea with blood, mucous or pus, fever, nausea, vomiting, stomach cramps, and wind that can last for days or weeks. Severe cases are treated with antibiotics.

Tularaemia

Insect: ticks, deer flies, horse fly, mosquitoes.
Organism: bacteria: Francisella tularensis

Francisella tularensis is present in a wide geographic band across the whole northern hemisphere. In areas where it is endemic, infections are seasonal and climate related, which may affect breeding conditions for vectors, though little research has been done, according to WHO. Many wild animals carry the disease and domestic cats are susceptible to infection.

The bacteria is highly infectious, needing only a few organisms to cause infection, though person-to-person infection is unknown. It can only survive in host cells where it depends on certain cell processes to survive.

There are several strains that vary in virulence and geographical range. Tularaemia is easily transmitted through the skin, mucous membranes, by direct contact with infected animals or animal materials, ingesting of contaminated food or water, and inhalation of contaminated dust or aerosols.

Each form of infection produces specific symptoms, usually inflammation and swelling at the site of infection, such as the eye, skin bite, lungs and swelling of nearby lymph glands. It can spread to multiple organ systems, including the lungs, liver, spleen, and lymphatic system, depending on the route of infection. It can be treated with antibiotics.

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Bibliography

Wikipedia: www.wikipedia.com

US Centers for Disease Control: http://www.cdc.gov/

WHO. Public Health Significance of Urban Pests. WHO, Copenhagen, 2008.

European Centre for Disease Prevention and Control: http://ecdc.europa.eu/

WHO. A global brief on vector-borne diseases. WHO, Geneva, 2014.

Cases of sleeping sickness drop to lowest level in 75 years http://www.who.int/trypanosomiasis_african/cases_drop_to_lowest_since_75_years/en/

WHO. Investing to overcome the global impact of neglected tropical diseases: third WHO report on neglected diseases 2015. WHO, Geneva.

WHO. Global strategy for dengue prevention and control 2012-2020. WHO. Geneva, 2012

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Graczyk TK, Knight R and Tamang L. Mechanical Transmission of Human Protozoan Parasites by Insects. Clin Microbiol Rev. 2005 Jan; 18(1): 128–132. doi: 10.1128/CMR.18.1.128-132.2005