Wolbachia mosquito initiative ready for global expansion

Aedes mosquitoes continue to expand their reach around the globe. Halting the spread of this nuisance is one piece of the jigsaw in the complex fight against dengue. Preventing these vectors from transmitting the virus is another. And that is exactly what the World Mosquito Program (WMP) aims to do.

We last spoke with the WMP around two years ago when we discussed how Wolbachia bacteria are reducing the impact of dengue. At that time, we examined how the WMP is using Wolbachia-infected Aedes mosquitoes to reduce the virus’ ability to replicate and mosquitoes’ ability to transmit the disease.

Expanding WMP operations

We recently spoke with Program Director Professor Scott O’Neill. He told us how, as a not-for-profit, the initiative’s goal is to “continue expanding to more countries as countries wish to learn about our technology.”

The initiative has made some significant progress in that direction over recent years. It has:

established an Oceania hub based at Monash University in Melbourne, Australia, and is now setting up its Asia regional hub in Ho Chi Minh City, Vietnam to help support countries locally as it expands its operations globally.
commenced releases of mosquitoes with Wolbachia in Kiribati, Fiji and Vanuatu and welcomed New Caledonia as the fourth country in the Pacific to commence a project.
announced that Mexico has become the first country in Central America to join the program, with La Paz set to be the first city to release Wolbachia mosquitoes.

The WMP is now releasing Wolbachia-infected mosquitoes in eight countries, with releases in India and Sri Lanka also in the pipeline. A total of 12 countries are embracing its approach, including, in addition to those countries already mentioned, also Australia, Colombia, Indonesia and Vietnam. “We’re hoping that within the next year or so we’ll be operating in 17 countries,” adds program director Professor Scott O’Neill.

Innovating for scale

As it deploys more projects in different locations around the globe, the WMP is continually learning and adapting its approach to improve how it releases its Wolbachia mosquitoes. Its goal is to become more efficient and more effective and to make its approach as affordable as possible. Optimising operations is not only key to expanding operations but also to reducing the cost of deployments – the WMP is targeting around US $1 per person protected.

The WMP recognised that it needed to understand how best to deploy the technology at scale. “Having done many successful small to intermediate-sized projects, we must learn how to deploy to cities of many millions of people,” says Professor O’Neill. “The challenges associated with operating at that size include mass production of mosquitos, deploying them most efficiently and scaling up community engagement.”

Starting with community engagement, the WMP has already adapted its approach to be more efficient at a larger scale. Professor O’Neill described how “community engagement is less intense than it used to be,” adding that the WMP was incorporating “more of our communications campaigns and less of the very intensive face-to-face community engagement” into its projects. He also confirmed that partners are helping to facilitate community engagement and that the technology is now seeing broad acceptance globally.

Efficient release operations

The community is also taking a greater role in actual mosquito releases. At the same time, the WMP is looking at alternative ways of releasing both mosquito eggs and mosquito adults efficiently at scale.

Its first unmanned aerial vehicle (UAV) trial got underway in Fiji last November in collaboration with not-for-profit WeRobotics and local experts, . “Although this work is in its very early stages, there is potential for UAV technology to help distribute mosquitoes with Wolbachia across large cities,” says the WMP’s Project Coordinator in Fiji, Mr Aminiasi Tavui, in a WMP news article.

As well as adapting how it releases its mosquitoes, the WMP is also refining where it releases them. “We used to release mosquitos everywhere in a target area,” said Professor O’Neill. “Now, through experience, we’ve realised that we only need to release them in a subset of areas to be effective; that also means we don’t need to release, and therefore produce, as many.”

Effective dengue blockers

Ensuring the Wolbachia-infected Aedes aegypti mosquitoes are effective at blocking the dengue virus – and therefore less likely to transmit it to the humans they bite – is critical.

A large-scale efficacy trial in Yogyakarta in Indonesia still has around a year left to run. While the study aims to rigorously evaluate the impact of Wolbachia bacteria on the transmission of dengue and other mosquito-borne diseases, the Professor confirms that in all locations the initiative is finding that “once we deploy Wolbachia at high levels, we see local dengue transmission collapse.”

We asked Professor O’Neill about his recent research into the susceptibility of Wolbachia-infected mosquitoes to dengue. The study found Aedes mosquitoes reared in the field were less susceptible to dengue infections than those it was rearing in its labs. He confirmed that “field mosquitoes are stronger dengue blockers than mosquitoes grown in the lab”.

He explained that this meant second-generation mosquitoes, the offspring of the laboratory-reared mosquitoes the WMP is releasing, are even better at halting dengue in its tracks. “It’s a really nice result to get,” he added. “It means our measurements from the laboratory of the potential impact of our technology are probably conservative.”

As the WMP continues to expand to more countries around the world, it is also exploring how it can also help in the fight against Zika, chikungunya, yellow fever and other viruses transmitted by Aedes aegypti.

We can’t wait to see how the WMP approach evolves in the coming months and years. We’d love to hear about your own novel approaches to halting dengue transmission. Contact us with your stories.

Science fights back in the war against dengue

With our climate warming, Aedes mosquitoes are spreading to new locations across the globe. The risk of dengue and other vector-borne diseases is rising. To fight back, scientist across the world are coming up with novel strategies for combatting the mosquito and the disease. Let’s take a look at a few of them, starting with the diet pills that aim to stop mosquitoes biting.

Diet pills could be the key to stopping Aedes aegypti mosquitoes from biting us, according to researchers at Rockefeller University in New York City. As you may be aware, only female Aedes mosquitoes bite. Understanding exactly why they nibble us led the researcher to this novel ‘diet pill’ approach to stopping the spread of dengue

Like other female mosquitoes, female Aedes bite us because they need the protein in our blood to produce their eggs. They only take what they need. Once they’ve had their fill, they won’t bite again until they’ve produced their eggs. But when they extract the small amounts of our blood that they require, they inject us with some of their saliva. Mosquitoes infected with dengue, pass the virus on.

Neurobiologist Leslie Vosshall came up with the wild idea that if we could trick mosquitoes into believing they had already had their fill of our blood, their desire to bite us would diminish. In her research, Vosshall fed some mosquitoes a solution of human appetite-suppressants and compared their behaviour to a control group. She found the mosquitoes given the ‘diet’ solution were far less inclined to seek out human scent than the control group.

Although it is early days in this research, initial findings are promising. If the method is ever used to suppress the appetites in the wild, it can’t rely on a drug intended for humans. An alternative would need to be developed that only affects mosquitoes to avoid any unintended side effects. If developed on a larger scale, it could potentially reduce how often mosquitoes bite and thus the spread of mosquito-borne diseases such as dengue.

Novel mosquito repellents

For our second example, researchers at the University of Wisconsin–Madison investigating new ways bacteria could be used to kill mosquitoes accidentally uncovered a compound that works as a mosquito repellent. They have taken that compound, which is obtained by purifying extracts of the microbes, and produced a mosquito repellent that is effective against a number of mosquito species, including Aedes aegypti. The repellent is still effective when used in lower doses than other repellents, making it potentially more cost-efficient. However, there is still a great deal more research to do in this area, and researchers haven’t established how safe these mosquito-repelling bacterial compounds are for humans.

It’s not only bacteria that scientists have resorted to in their quest to deter mosquitoes. Lavender is a plant loved by many for its scent and medical properties. One of its other properties is less well-known: it’s also a mosquito repellent. In a bid to discourage Aedes mosquitos, leaders in the Marunda area of North Jakarta have turned to lavender for help, planting 2,000 of the purple flowering shrubs. The Marunda community has already formulated a second plan for eliminating the mosquitoes: introducing betta fish to their ponds to feast on mosquito larvae – a technique similar to the use of guppy fish we’ve written about.

A number of natural mosquito repellents are also becoming commercially available. Cinnamon oil, for example, has been shown to kill mosquito larvae. Researchers in Taiwan have previously suggested that the product could be a better-smelling alternative to established chemical pesticides. A Sri Lanka-based company, Cinnamon Hill, is marketing an insect repellent spray made with cinnamon leaf and bark oil, while lemon eucalyptus oil, lavender and neem oil are also commonly used.

Mosquito birth control

Our fourth and fifth approaches look at ways of reducing Aedes populations using new forms of mosquito birth control. Research carried out at the University of Arizona and San Jose State University manipulated a specific gene code (a set of rules by which information encoded in genetic material is translated into proteins) that they believe plays a vital role in the formation of mosquito eggs. During their research, the team bred some female mosquitoes with a disrupted gene code for the EOF1 protein. The results showed that the majority of eggs produced from these females were unviable. Most significantly, the EOF1 protein is unique to mosquitoes and, therefore, any insecticide produced to target it would be less likely to be harmful to other life forms.

University of Florida researchers are also looking into reducing the mosquito population through a form of birth control, this time exploring a technique known as ‘satyrization’. Here a male mosquito from one species mates with a female from a different species. When satyrization occurs, the female is unable to produce the hybrid offspring. Not only is her egg not fertilised, but her reproductive system becomes infertile.

While researchers hoped cross-species mating between Aedes aegypti and Aedes albopictus in regions where the two types of mosquitoes co-exist might reduce the mosquito populations, their studies revealed that mosquitoes learn to avoid cross-species mating within a few generations. They also found that when the species where separated, the mosquitoes lost all they had learnt within six generations. There is still more research to be done. New insights could help us predict how Aedes populations interact as they invade new regions.

Fighting dengue infection

Looking beyond mosquito birth control to treating dengue infection, an article published by Lahore University of Management Sciences suggests a common natural spice could offer a breakthrough in dengue treatment. Cloves contain eugeniin, a chemical thought to have the ability to halt the production of dengue viral components. Eugeniin could potentially prevent the creation of a mature dengue virus, halting its ability to replicate.

With so many potential new tools emerging in the fight against dengue, we’d love to hear about your own novel research or techniques in your own battle against the disease and its Aedes vector.

Tokyo Olympics, public health, and the threats posed by Aedes albopictus

The Tokyo Olympics and other mass gatherings provide the perfect opportunity for many dangerous vectors. Sporting, religious and cultural events often attract large numbers of people from different parts of the world, bringing with them both vectors themselves and the viruses they carry. With Tokyo’s preparations for hosting the 2020 Olympic and Paralympics Games in less than 18 months well underway, we explore the risk of a dengue outbreak during the games, drawing parallels with the Zika threat during the 2016 games in Brazil. Let’s begin by taking a look at the status of dengue and its Aedes vector in Japan.

At a global level, the Asian tiger mosquito (as Aedes albopictus) is a secondary, yet still very important, dengue vector. It’s the main dengue vector invading temperate and semi-temperate countries; its spread fuelled by an increase in global travel and the used tire trade. Yet very dry and very cold weather, along with improvements in the way unwanted materials (such as used tires) are handled, is preventing the mosquito from establishing itself in some areas – inhibiting its march forward.

Aedes albopictus has been present in Japan for some time. According to the Journal of Medical Entomology:

“During World War II, conscripted ships brought dengue fever into Japan from epidemic areas, and it became prevalent in the western parts of Japan.”

A research article published in 2015 highlights Japan as one of the top ten countries for Aedes albopictus mosquitoes. Researchers confirmed the mosquito’s presence in an article published in Geospatial Health a year earlier, in 2014:

Map showing recent Aedes albopictus mosquito activity in Japan.

Distribution of Ae. albopictus confirmed areas in the Tohoku region of Honshu in 2012 and the northern limit of Ae. albo-pictus. (b) Mosquito collection sites in Yamagata city (1998-2010) via Geospatial Health

Dengue in Japan

With Aedes albopictus established in Japan, dengue outbreaks are a real possibility. Japan experienced an unexpected outbreak during the summer of 2014, the country’s first autonomous transmission for 70 years.

The videos published in this 2014 research article show that Japan’s climate would allow Aedes albopictus to transmit the dengue virus during the summer months:

Map showing the Aedes albopictus temperature suitability for the introduction of dengue transmission, a Tokyo Olympics public health risk.

Aedes albopictus temperature suitability for the introduction of dengue transmission throughout an average year. Source: Parasites & Vectors

And allow Aedes albopictus to maintain that transmission during the summer months:

Map showing the Aedes albopictus temperature suitability for the introduction of dengue transmission, a Tokyo Olympics public health risk figure two.

Aedes albopictus temperature suitability for the persistence of dengue transmission throughout an average year. Source: Parasites & Vectors

The dengue threat to public health during the Tokyo Olympics

Japan is in the midst of preparing to host the 2020 Summer Olympics and 2020 Summer Paralympics in Tokyo. The games will take place during the summer months when temperatures can rise to over 30 °C, raising the risk of dengue transmission.

Despite the fact that dengue and tourism can be an unhealthy combination, millions of people from Japan and all over the world are expected to attend the games. The host city will welcome thousands of athletes along with staff, officials, volunteers, and spectators. The large influx of people poses potential health risks, including a heightened risk of dengue.

With Aedes albopictus established in Japan, the country must prepare to counteract any dengue threat during the games. It finds itself in a situation similar to that faced by Brazil ahead of the 2016 games. Brazil 2016 took place as Zika spread rapidly across South and Central America. Zika, like dengue, yellow fever, and chikungunya, can be spread by Aedes mosquitoes.

Zika threatened the Brazil Olympics

The games were due to take place in August 2016, during the Brazilian winter. Just over a year earlier, in May 2015, Brazil reported its first ever case of Zika. The virus spread rapidly. The World Health Organization (WHO) declared the outbreak a Public Health Emergency of International Concern (PHEIC) – a danger to international public health – in February 2016.

With the Olympics close, a research article published in March of that year included recommendations for those attending the games:

“Measures to avoid mosquito bites include wearing long-sleeved shirts, use of insect repellent and staying in screened or air-conditioned accommodations. … Control efforts so far rest entirely on mosquito vector control both at community and household levels and prevention of mosquito bites by individuals.”

There were some calls for organizers to cancel the games. But, in June 2016, the WHO Zika emergency committee concluded that the risk of further international spread of Zika was very low because the games would be taking place during the Brazilian winter. It advised, among other things:

Brazil should continue its work to intensify vector control measures and enhance surveillance for the Zika virus and its mosquito vector around cities and venues hosting events, publish information in a timely manner and ensure sufficient insect repellent is available.
Countries with travelers to and from the games should ensure travelers are fully informed on the risks, personal protective measures and action if they suspect infection. Countries should also establish protocols for managing travelers returning with Zika.

Three months later, in September 2016, the committee congratulated Brazil on its successful application of appropriate public health measures during the Olympic Games, confirming “There have been no reports of confirmed cases of Zika virus among people who attended the Games, both during the games and since their return.”

Dengue advise for Tokyo 2020

With the Tokyo games drawing ever nearer, researchers have examined the public health implications of several potential threats, including dengue. They shared their thoughts in an interview with the International Society for Neglected Tropical Diseases (INSTD), concluding “current controls for dengue detection which include guidelines and services to update both physicians and travelers on infections are robust”.

During the discussion, the researchers noted their views on the main public health challenges at mass gatherings:

The introduction of a new or non-endemic infectious disease.
Stretched health systems may strain existing surveillance systems.
Political/media interest and rumors may magnify anything negative.
A multi-sectoral approach is essential to mitigate the risks.

In terms of dengue, they recommended: “Continuous efforts are needed to maintain awareness of dengue and strengthen the capacity of infectious disease control.”

Mass gatherings are also a golden opportunity for raising awareness around neglected diseases such as dengue. Have any of the mass gatherings you’ve attended turned up the volume on dengue?

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Tourism and dengue: A look at the effect of an unhealthy combination

For countries that depend on tourism, the economic cost of a dengue outbreak can be substantial. Afraid of catching the virus, tourists and their dollars stay away. But where are tourists learning about dengue outbreaks? Why are they staying away? And what is the real economic impact of a dengue outbreak? Let’s explore how dengue is affecting tourism.

We live in a world where tourists looking for a relaxing break have access to a wealth of information about their destinations. They simply turn to the web to find out about their planned destination. With search engines able to quickly gather information from many different sources, they quickly learn about any a dengue outbreak. The web also helps them learn not only about the virus itself but also how to minimize the risk of being bitten by an infected mosquito, what symptoms to look out for and much more.

Tourists warned about dengue activity

Firstly, they may find a multitude of official travel sources from governments and travel authorities around the world. These warn tourists of the potential risks of traveling to dengue-endemic countries.

The US Centre for Disease Control (CDC) warns:

“Travelers who go to tropical and subtropical regions are at risk of getting dengue. These areas include parts of the Caribbean, Central and South America, Western Pacific Islands, Australia, Southeast Asia, and Africa.”

The NHS ‘Fit for Travel’ website warns:

“Dengue fever is widespread throughout the tropics and subtropics, occurring in > 100 countries. Nearly 100 million clinical cases of dengue fever are thought to occur every year.

“Dengue is the second most commonly identified cause of fever in ill international travelers.”

Fit for Travel also provides relatively up-to-date information on current dengue outbreaks. The NHS website also advises tourists of the on-going outbreak in Sri Lanka: “According to media, the Sri Lankan Ministry of Health has reported 4,825 cases of dengue fever, including at least 2 deaths, in the first four weeks of 2019. …all travelers to regions where dengue occurs are potentially at risk of dengue fever and should be aware of this infection.”

And the on-going outbreak in Jamaica: “The Jamaican Ministry of Health has issued an outbreak alert following an increased number of dengue cases in December 2018. During that month, 123 cases of dengue were recorded in the country.”

Similarly, Health Travel Pro (travel health resources from the National Travel Health Network and Centre (NaTHNaC)) points tourists to factsheets on diseases along with news of outbreaks, recently highlighting an increase in dengue cases in Kenya.

Read more about dengue in Africa

Tourists can quickly and easily discover where dengue outbreaks are, how severe they are, and what local authorities are doing to combat them.

The online discussion around tourism and dengue

But it’s not only government and travel websites where tourists can learn about dengue outbreaks; they are also very active in discussing dengue on online forums, especially those set up by travel booking websites. When we searched for the term ‘dengue’ on TripAdvisor website, we found the disease mentioned within hotel and resort reviews:

And that it was also a very active topic of discussion on the website’s forums:

We delved deeper into a discussion on the 2019 dengue outbreak in Jamaica on Trip Advisor to find out what the conversation looked like. It started with someone raising concerns about traveling to Jamaica with their family during the outbreak:

The comment received nine replies in just a day and a half. Replies from other users included pointers to recent media stories covering recent dengue outbreaks in the country with some users people giving reassurance. The risk of dengue clearly influences tourists when they are choosing where to spend their holidays – and their dollars.

Dengue’s economic impact on tourism

With not only governments and travel advice websites warning tourists of the risk of dengue but also their peers, what impact might a dengue outbreak have on a region? The economic impact of dengue could be significant for a region that depends on tourism.

There have been numerous studies into the economic cost of dengue, with some explicitly delving into its impact of the disease on tourism:

An article on the effect of dengue in tourism in Brazil concluded that “tourism revenue losses are significant, impacting the country economy and GDP” during a dengue outbreak. Researchers drew their conclusions by analyzing data from Brazil’s 2013 dengue outbreak, a year when the country saw almost 1.5 million suspected dengue cases according to PAHO data. They estimated “a conservative decrease of 4% in tourism in Brazil due to the dengue outbreak” with “an economic impact of US$132.3 million from international tourism and US$1.4 billion from local tourism”.

A more recent economic analysis of dengue prevention and case management in the Maldives concluded that the risk of dengue lowers the country’s gross annual income by a $110 per resident and its annual tax receipts by $14 per resident. Noting that tourism is the mainstay of the Maldives’ economy, it calculated that tourism generates an “annual income of $898 and tax revenues of $119 per resident”.

We can only conclude that dengue outbreaks influence where tourists choose to spend their holidays. With their dollars finding their way to countries where the risk of disease is lower, the economic impact can be significant.

Has your country experienced a fall in tourist numbers during or following a dengue outbreak? How did it react? We’d love to hear about the measures it took to combat the disease and to bring tourists back. What impact did these have?

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Dengue trends in the Caribbean and the Americas during 2018

The dengue trends across the Caribbean this year have PAHO expressing concern for the region, but looking back at the Americas during 2018, there was mixed news on dengue.

The region reported 6,418 suspected dengue cases in 2018, down from the 7,460 in 2017. However, deaths were up at seven in 2018 compared with three in 2017. The worst hit were countries were Jamaica (986 dengue cases and six deaths in 2018 up from 215 cases in 2017), Cuba (2,128 dengue cases and one death in 2018 compared with 1,248 cases in 2017) and the Dominican Republic (1,558 dengue cases in 2018 compared with 1,363 case and three deaths in 2017).

The 2018 dengue trends case numbers in the Americas continued a downward trend from 2017. By the end of the year, dengue case numbers across the Americas had reached just below 540,000 compared with more than 580,000 in 2017, almost 2.2 million in 2016 and more than 2.4 million in 2015. Dengue in the USA followed the trends with 331 dengue cases in 2018, down from 453 in 2017 and 990 in 2016.

A map of the Americas showing dengue activity in 2018.

Image via PAHO

Brazil continued to account for almost half of those dengue cases, with numbers similar to 2017: almost 247,000 dengue cases with 141 deaths in 2018 compared with just over 252,000 cases with 133 deaths in 2017; 1.5 million cases with 642 deaths in 2016 and almost 1.65 million cases with 863 deaths in 2015. In 2015, Piracicaba began releasing Oxitec’s Friendly Mosquitoes (Aedes do Bem) to combat dengue. This followed pilot studies in Juazeiro and Jacobina between 2011 and 2015. Juiz de Fora began releases in November 2017.

Dengue up in some regions of the Americas

Argentina, Chile, Colombia, El Salvador, Guatemala, Guyana, Honduras, Paraguay, and Venezuela all reported rises. With all four dengue virus serotypes circulating, the risk of severe dengue was also increased from 0.36% in 2017 to 0.65% in 2018 as has the risk of death at 0.058% in 2018, up from 0.054% in 2017 and 0.042% in 2016.

Chart showing the dengue trends in the Americas in 2018.

Image via PAHO

Argentina reported a trebling of dengue cases, with 1,829 in 2018 compared with 557 in 2017. The number included 1,164 confirmed cases. There were no cases of severe dengue and no deaths either year.

Dengue cases jumped significantly in Paraguay with more than 32,359 dengue cases, including 3,414 confirmed cases, reported in 2018, up from 1,832 cases and 616 confirmed cases in 2017. Case numbers included 15 dengue-related deaths in 2018, up from no deaths in 2017. Numbers were still much lower than the 70,215 dengue cases reported in 2016 but on par with the 16 deaths that year.

Colombia also experienced a sharp rise in dengue cases in 2018. The country’s health system received notification of 44,825 cases, including 526 of severe dengue and 23 deaths. This compares with 26,279 cases and 15 deaths in 2017.

Dengue numbers also rose in El Salvador, though actual numbers are difficult to decipher. According to the country’s Ministry of Health, 458 probable cases were reported during 2018, an increase of 197% on the 154 cases reported in 2017, with eight fatalities. These numbers are significantly lower than the 8,488 dengue cases in El Salvador reported by PAHO.

In Honduras, dengue case numbers reached alarm levels between late March and mid-May of 2018. A total of 7,942 suspected cases of dengue were reported throughout 2018, including 1,172 cases of severe dengue and three deaths. In 2017 there were 5,217 and no deaths.

The number of dengue cases more than doubled in Venezuela with a total of 19,118 dengue cases notified, of which 2,440 were confirmed. This compares with 8,615 reported in 2017. Nationally, there were 24 dengue deaths in 2018, up from 16 in 2017.

Stay tuned for our final part of our three-part series looking back at dengue in 2018, we will look at how Africa and Europe fared.

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Dengue is spreading across Africa and it’s making its way into Europe

Dengue is spreading its reach around the globe. In 2019, we’ve taken a closer look back at the 2018 dengue season across the Asia Pacific and the dengue trends in the Caribbean and in the Americas. We brought news of fresh outbreaks across both regions as well as stories of new strategies to help countries to respond to the dengue threat. The story for both Africa and Europe was more negative with outbreaks spreading to new locations. Find out how dengue impacted the continents’ countries in 2018.

New dengue outbreaks in Africa

Dengue in Africa became more and more common during 2018. Across the continent, new outbreaks were reported in Senegal, Mauritania, Ethiopia, Tanzania, and Angola, adding to the ongoing outbreak in Seychelles. Meanwhile, Burkina Faso’s 2017 dengue outbreak subsided early in 2018.

Angola in 2018 with five dengue deaths out of a total of 1,339 cases as of late October 2018 – the largest outbreak in the country since 2013 when 1,245 cases were recorded, with 11 deaths. The country recorded only 66 cases and one death in 2016, and 176 cases with four deaths in 2017.
As of late October, Seychelles had reported 6,120 dengue cases since its dengue outbreak began in December 2015, with 1,511 of those confirmed. While case numbers slowed between June and August, they had started to rise again by late October.

Dengue cases were down in Burkina Faso in 2018 compared with the 15,096 dengue cases and 30 dengue deaths in 2017. Dengue numbers had begun to decrease in the last quarter of 2017; during the first quarter of 2018, Burkina Faso reported 909 suspected cases and three deaths.

Elsewhere, the Senegal Ministry of Health declared its outbreak over towards the end of December after 2,981 suspected dengue cases, with 342 of those confirmed. Dengue was reported in Tanzania in the first half of 2018, with 226 cases with no deaths. An outbreak of dengue in Ethiopia started in June and involved 127 suspected cases. Mauritania reported 322 dengue cases with no deaths during October and November.

Dengue is spreading into Europe

The threat of dengue in Europe is also on the rise. Health authorities in the EU reported locally-acquired cases of dengue in France and Spain during late 2018.

Spain reported six locally-acquired dengue cases from three different regions during the second half of the year. Three cases were members of the same family, first experiencing symptoms late in August after spending time together in Murcia and Cádiz. The Catalan Public Health Agency (ASPCAT) confirmed its first case of autochthonous dengue early in November. Murcia also reported two dengue cases in November.

Similarly, France reported eight locally acquired dengue cases from three different regions during the second half of 2018, in addition to 189 imported cases: five dengue cases were detected in the Alpes-Maritimes department in September and October 2018; two cases occurred in the Hérault department at the end of September and beginning of October; one further case of dengue was identified in the Gard department in October.

Did your country experience a new dengue outbreak in 2018? How did it start? How did people react?

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Dengue season across Asia and the Pacific Islands. Is climate change prolonging its length?

“Dengue season” is a relative term used by many health officials around the globe. But in many countries where the disease is endemic, dengue season is getting longer, and more intense.

Last year, countries across the world felt the effects of our world’s changing climate: soaring temperature set records across the globe, terrible flooding hit parts of India and a super typhoon caused devastation in the Philippines. The unusual weather brought dengue outbreaks to many Asia Pacific nations, while novel technologies helped others to fight back. Let’s explore the dengue highs and lows experienced by Asia and the Pacific Islands in 2018.

dengue season outbreaks. Map of Asia Pacific showing dengue activity.

Image via ReliefWeb

Asia’s dengue lows indicate cases are on the rise

Cases of dengue in Thailand in 2018 were up compared with 2017 with official sources reporting a total of 54,482 cases and eight deaths across 77 provinces. Other reports put case numbers over 80,000 and fatalities above 100.

2018 was being called the deadliest year for dengue fever in Bangladesh with 17 deaths by late November and nearly 10,000 dengue cases as of early December. The spike of 3,087 cases reported in September, towards the end of Bangladesh’s monsoon and peak dengue season, was more than double previous years.

The Philippines recorded a 33% rise in dengue cases compared with 2017, with 179,540 cases reported nationally from the beginning of the year through mid-November. Close to a thousand dengue deaths had been recorded by mid-November. The flooding following typhoons contributed to the increase in dengue cases.

Singapore is expecting a surge in dengue cases in 2019 thanks to the 40% increase in the Aedes aegypti population seen in December compared with December 2017. The National Environment Agency (NEA) reported the total number of dengue cases in 2018 as 3,285, a 20% increase on 2017 but lower than in earlier outbreak years.

Cambodia reported a 50% rise in dengue cases and deaths in the first 11 months of 2018 compared with 2017, with 15,233 cases and 16 deaths. The dengue epidemic period peaks from May to October in Cambodia.

Dengue cases began rising in Malaysia mid-September. A total of 5,003 dengue cases including twelve deaths were reported in the last two weeks of 2018, bringing the annual total to 80,615 and 147 deaths, as of 29 December. This contrasts with the downward trend seen from mid-September in 2017.

Graph showing the rise of dengue cases reported weekly in Malaysia in 2017 and 2018.

Dengue cases reported weekly in Malaysia in 2017 and 2018 via W.H.O.

The island of Flores in Indonesia saw a sharp increase in dengue cases from 161 in 2017 to 539 in 2018, with 441 of the cases reported between September and December. Indonesia is home to one of the many Wolbachia programs in Asia to curb dengue outbreaks. The World Mosquito Programme began releases of Wolbachia mosquitoes on the island of Java in small trials in 2011 and is currently in the midst of a large-scale efficacy study to evaluate their impact. In 2019, Indonesia has already seen over 100 dengue deaths in January alone.

The WHO country office is supporting the response to the current outbreak of dengue in Pakistan. As of early January 2019, there have been 16,580 confirmed cases and 257 deaths reported in capital Lahore and nearly 5,000 cases and 60 deaths reported from the rest of the country.

Elsewhere, Oman recorded 67 dengue cases towards the end of 2018, 30 of them imported. France’s Réunion Island’s dengue epidemic had reached 6,712 cases and three deaths by late December.

Asia’s dengue highs: The fight shows its muscle

Official statistics show a worsening dengue situation in India. As of late November, there had been 89,974 cases and 144 deaths across the country. Numbers for the year are most likely going to be down compared with 188,401 cases and 325 deaths in 2017. The WMP is currently undertaking laboratory studies Wolbachia-infected mosquitoes in India.

Sri Lanka saw a substantial decrease in dengue cases in 2018 with 51,271 cases compared with 186,101 cases in 2017, which was one of the country’s worst-ever outbreaks of the disease in recent years. There were also 56 dengue fatalities reported in 2018 Early in 2018, the National Dengue Control Unit launched special programmes to eradicate dengue breeding grounds in several districts of the island country

From March until June last year, WMP carried out its first releases of Wolbachia mosquitoes on mainland Vietnam. Elsewhere around Vietnam, dengue has been taking its toll. Ho Chi Minh City saw a 125% increase in dengue cases in October compared to a year earlier with the city’s hospitals admitting 4,390 people with the disease that month. Late in September Hanoi reported a sharp drop in dengue cases (down 96.8%) compared to the first nine months of 2017.

Australia reported 824 dengue cases in 2018, which was down on previous years. For instance, Queensland reported 212 confirmed dengue cases in 2018 compared with 292 in 2017 and 445 in 2016.

Dengue in the Pacific islands in 2018

Surrounding dengue in the Asia Pacific region, New Caledonia declared dengue outbreaks in February and again in December with nearly 2,000 cases and two deaths by late December. The French territory of the Wallis and Futuna Islands reported a total of 225 dengue cases and one death between September 2017 and early January 2019; Wallis has recently raised its dengue alert level. In December, Palau declared a dengue outbreak following the first ever laboratory confirmation of two
Cases.

In better news, French Polynesia raised a dengue alert in June after two cases were confirmed, then lifted it in August. Fiji dengue case numbers began falling towards the end of May, with 3,437 cases and four deaths at that point. And an early 2018 dengue outbreak in Vanuatu had weakened by late March after 329 suspected and 52 confirmed cases.

With funding and support from the Australian Government’s InnovationXchange, the WMP announced in August release of Wolbachia mosquitoes in the Pacific in Kiribati, Fiji, and Vanuatu.

Do you live or work in the Asia Pacific region? We’d like to know what changed during dengue season in your community during 2018. Share your story with our editors.

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The threat of dengue in Europe and how the continent is reacting

The threat of dengue in Europe has become a reality. At the tail end of 2018, autochthonous dengue cases appeared in Spain and France, and its vector, Aedes albopictus, has spread ever further north and was recently reported in Eindhoven. The lesser-known and less capable vector Aedes japonicus is expanding its presence across central Europe. But, most worryingly, the climate and environment remain favorable for primary vector Aedes aegypti to become established once more. We spoke with two experts involved in EU-funded Actions to combat Aedes and dengue: Dr. William Wint, Senior Research Associate in the Zoology Department at Oxford University, and Dr. Giulio Nannetti, Post-Doctoral Research Associate in the School of Pharmacy and Pharmaceutical Sciences at Cardiff University to learn more about the threat of dengue in Europe.

Map showing the June 2018 distribution of Aedes japonicus in Europe.

Image via the ECDC

Our first conversation focused on dengue vectors: mosquitoes in the genus Aedes. Dr. Wint began by explaining the current status of Aedes in Europe: “The Asian tiger mosquito has been spreading in Europe for more than two decades. It’s a real nuisance that spreads very quickly and is now recorded in most of the EU. Aedes japonicus came into Europe more recently and is spreading in all directions from south-central Europe, where it was first introduced. It is also spreading northwards in Germany, reaching the latitudes of south-central UK.”

Aedes aegypti largely vanished from Europe in the 1950s, possibly because piped water introduced after the war led to a decline in the rain butts and other water containers that were the main breeding sites for its larvae. “The European climate remains suitable for the vector, indeed increasingly so, and it’s now spreading west along the Turkish Black Sea coast,” said Dr. Wint. “Why it hasn’t yet found its way back into the rest of the EU is a real mystery”.

The AIM COST action

Dr. Wint leads one of the three working groups set up by the Aedes Invasive Mosquitoes (AIM) COST Action, an initiative funded by COST (European Cooperation in Science and Technology) to build a network of European stakeholders to strengthen Europe’s capacity to combat Aedes mosquitoes, and the spread of dengue in Europe. The action, according to COST, will “assess and review current surveillance, control, and analysis practices, develop best practice guidelines and protocols ensuring consistency across Europe”.

“Aedes are competent vectors of a range of diseases,” said Dr. Wint. “It serves us well to harmonize the guidelines for surveillance and control within Europe; if people do things differently – do surveillance at different times of the day or use different numbers of samples, for instance – it’s much more difficult to build a comparable picture of what’s happening across the continent.”

The project may also tailor the guidelines so more people can understand what needs to be done and, in some cases, help with control or surveillance efforts.

A broad spectrum of participants

Beyond developing guidelines, the AIM COST action will also measure its success on building and sustaining relationships, organizing funded projects and increasing understanding of the action, its activities and the status of Aedes in Europe. Bearing these in mind, the breadth of participation is not surprising.

The network is run by Alessandra della Torre, Associate Professor at the Sapienza University of Rome in Italy, and Professor Dušan Petrić from the University of Novi Sad in Serbia. It is primarily made up of entomologists, many of them early in their careers, alongside experts in dengue genetics, in mosquito control and surveillance, and in mapping. Its management committee comprises two qualified professionals as national representatives from each of the 35 countries involved. Dr. Wint represents the UK alongside Dr. Jolyon Medlock from Public Health England, for instance.

International agencies, such as the European Centre for Disease Prevention and Control (ECDC), the World Health Organization (WHO) and the European Mosquito Control Association, will also participate, alongside other national agencies and organizations.

“We’re also hoping to get ordinary people involved through Citizen Science,” says Dr. Wint. “We need feedback on how important people think this is. We also want to keep the public informed and to ensure anything anyone does is compatible with the more formal things scientists and technicians do.”

Reducing the threat of dengue in Europe through focused workgroups

One of the action’s first tasks was forming three work groups, each with a distinct role: one developing the harmonized monitoring/surveillance guidelines, one developing the harmonized control guidelines and one, which Dr. Wint leads, making sure that the work the other groups produce gets out into the real world. Dr. Wint tells us his group will “go out and find out what people expect of the guidelines, how they want them presented, who they should go to … even find out whether the maps produced by the other two work groups are in the right colors and format.”

The project also has a Science Communication officer whose role is to ensure the information reaches the right places and “not just journals or agencies but to a much broader audience.” Social media will play an important role.

The four-year project kicked off in September with a meeting of national representatives in Brussels, at which the leaders of the action’s three workgroups revealed and gained buy-in for their plans. The first AIM-COST Annual Conference is scheduled to take place in Athens from 12th – 14th February.

Our second conversation focused on dengue itself – more specifically the development of a new treatment aimed at preventing dengue infections from progressing to severe forms of the disease.

Developing a new dengue treatment

With the prospect of dengue arriving in Europe, Dr. Nannetti is working under the supervision of Professor Andrea Brancale on an EU-funded project to develop innovative broad-spectrum antiviral compounds to combat all four serotypes of the dengue virus. “The lack of specific treatment for dengue fever makes the development of new anti-dengue strategies critical,” says Dr. Nannetti. “They would have an enormous impact on public health worldwide, potentially preventing significant costs and economic loss.”

Group photo of the team at Brancale's lab fighting the threat of dengue in Europe.

Image: The team at Brancale’s lab fighting the threat of dengue in Europe.

Funded under the Marie Skłodowska-Curie Actions, the University of Cardiff FINDER (FIghtiNg DEngue virus) project is partnering with the laboratory of Professor Arianna Loregian at the University of Padova in Italy to find a way to stop the dengue virus from replicating, using an approach similar to one he previously used to develop anti-flu compounds.

It has previously been observed that higher amounts of the dengue virus (or a higher viral load) in patients’ blood patients increases the risk of developing severe disease. That observation suggested that a good dengue antiviral could limit and revert the progression of the disease.

“We aim to disrupt the interaction between viral proteins that the dengue virus needs to replicate,” says Dr. Nannetti. “We have, to date, used computer-aided drug design approaches to identify a promising druggable target (a portion of a virus protein that can be bound well by a drug) for all four dengue serotypes.” The team used the target as a template to screen for compounds that could potentially inhibit the dengue virus and are now testing these molecules.

Image of the dengue NS3 protein courtesy of Dr. Nannetti

Drug development is a long and complex process that can take more than a decade. By the end of his two-year fellowship, Dr. Nannetti expects to have identified one or more non-toxic candidate drugs capable of interfering with the dengue virus replication in cellular systems. “Next steps would then be to evaluate the antiviral activity of these anti-dengue candidates in preclinical models,” he concludes.

If you’re working to combat the threat of dengue in Europe or developing novel treatments to combat the dengue virus itself, please get in touch. We’d love to hear from you.

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Dengue Illness Index: Giving patients a voice on the true burden of dengue

It’s nearly five years since the International Federation of the Red Cross (IFRC) published its report Dengue: Turning up the volume on a silent disaster, which in part explores the burden of dengue. Noting that “approximately 60% of dengue-related costs are not directly associated with healthcare expenditure”, it highlights the indirect costs borne by patients and their families: “On average, between 14.8 and 18.9 days are lost as the patient is incapacitated or a family member needs to stay at home.”

All too often, costs, complex logistics and an inability to capture data in a manner acceptable to regulatory agencies. As a result, clinical trials for dengue vaccines and treatments ignore these aspects of the burden of dengue in their deliberations. The Dengue Illness Index (DII) hopes to change that.

“Trials typically measure a couple of days of fever and a positive dengue test, or hospitalization and/or severe disease. Clinical scenarios in between may still be relevant,” says Professor Stephen Thomas, Director of the Institute for Global Health and Translational Sciences at the State University of New York Upstate Medical University. “There’s clinically relevant disease occurring that a vaccine or drug might impact. The people who make decisions about licensing or using vaccines would benefit from understanding that impact – but researchers are challenged how best to measure it. We haven’t figured out how to.”

The true burden of dengue

Researchers know how much is being spent and what the clinical outcomes are for people hospitalized with severe dengue. But most people with dengue are managed as outpatients. “Even though it’s not as clinically severe, the burden of outpatient dengue, when you consider all of its impacts on the individual and the family, is considerable and from some perspectives more than the burden of inpatient dengue,” says Professor Thomas.

He gives an example of a child home from school because they have dengue: “They’re not sick enough to be admitted to the hospital, but they cannot attend school. Therefore, someone needs to stay home with the child, which means this person may lose a day’s pay since they cannot go to work. The child may need frequent assessments as an outpatient, which means paying for transportation, perhaps the doctor’s visit, maybe a blood test, food and perhaps medication such as paracetamol. You can see where the economic cost of dengue can become significant, especially for people who are economically disadvantaged.”

During vaccine trials, researchers have to capture endpoints that are objective and reproducibly measurable across many regions to assess vaccine safety and efficacy. Assessing fever and testing the blood for evidence of a dengue virus infection is the current standard. Later in trials, the researcher may only assess hospitalized cases. By approaching studies in this way, there may be an entire spectrum of clinically relevant disease that is not being evaluated and, as such, there is a missed opportunity to expand the perspective on the potential impact of vaccines or drugs.

“What if you could measure these relevant but often not measured patient experiences?” asks Professor Thomas. “If the person who had a placebo had a four-day illness experience and a person who had the vaccine had a two-day illness experience, the overall clinical severity would have been shifted towards a less severe disease scenario and, by extension, the overall individual and public health impact would have been mitigated. When you’re talking about an estimated 96 million symptomatic dengue virus infections each year around the globe, this impact could be substantial. I propose we explore how to measure what is currently a grey area.”

Researchers need to understand whether experiences differ between those receiving a placebo or control and those receiving the experimental product. To gain new perspectives on the potential benefits of vaccines and drugs, they need to give the vaccine recipient a voice.

A dengue index for researchers

Back in the ‘80s and ‘90s, the professor’s mentors, including his current partner in the project Dr. Robert Edelman from the Center for Vaccine Development at the University of Maryland, developed a ‘dengue severity index’. During trials, they would ask volunteers whether they had any symptoms, then grade the severity by assigning numeric values. Professor Thomas explains how the final number “helped them gauge which volunteers were having unacceptable adverse reactions to the vaccines and their severity and whether the vaccine candidates were suitable and appropriate for further clinical development.”

The World Health Organisation also developed its own dengue severity classification in the late ‘90s, updating it in 2009. Professor Thomas makes a point, however, that the WHO indices are distinctly different from his and Dr. Edelman’s proposal. The Illness Index was developed to support clinical research, not clinical care, and does not intend to classify severity.

Fast forward 15 years. Professor Thomas was attending a conference co-sponsored by the US National Institutes of Health where the intention was to re-look at classifying dengue severity to support research initiatives. It was here that Drs Thomas and Edelman began to work together on updating the severity index. “We pulled the previous index off the shelf and reworked it,” says Professor Thomas.

The new index was designed to give patients a voice: What symptoms do I have? How bad are they? What impact is dengue having on my daily activities? Can I assign a numeric value to this experience for comparisons between people and groups?

DII: Measuring patients’ experience of dengue

The Dengue Illness Index (DII), as the professor’s paper, describes, “was developed to improve and standardize the measurement of vaccine and drug efficacy in reducing moderate dengue illness by capturing the overall subjective disease experience of an individual based on how the totality of their symptoms impacts their wellness and daily functionality.”

In other words, it’s a tool for capturing the patient’s experience of dengue (rather than characterizing dengue severity) that is intended to support research (rather than clinical management of the disease). The information it provides could be valuable for understanding the impact – or lack of impact in some cases – of either preventative or therapeutic drugs or vaccines.

“The Dengue Illness Index aims to help us understand what the person with dengue is experiencing and how it impacts their overall functionality,” says Professor Thomas. “We are currently using it in a prospective dengue study in the Caribbean.”

The SUNY Upstate Medical University in New York, where the professor works, will be using the index during 2019 in its experimental human infections to support the dengue vaccine and drug development.

Regulatory approval for the Dengue Illness Index

A large pharmaceutical company is also investing in the DII, taking it to the next level. “Putting it into a Patient Measured Outcome (PMO) format that would generate data of sufficiently high quality for a regulatory agency to accept,” reveals Professor Thomas.

The updates could take almost 18 months. According to the professor, for regulatory authorities to accept the index, questions need to be asked in a way that ensures researchers don’t introduce bias. The index must also be cross-cultural, cross-language and easy to sell to volunteers. “It has to be in a platform that people are willing and interested in filling out,” he says.

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The pharmaceutical firm also intends to make the Dengue Illness Index available to others. In the longer term, Professor Thomas would like to see the index provided in a web-based format that people could access with their phone. “Pushed to a volunteer with the information gathered going into a cloud,” he concludes.

We can’t wait to see how the Dengue Illness Index will evolve in the coming months and years. Get in contact with us if you are working on your own version of the index.

And we’d also love to hear about your personal dengue experiences. How did this terrible disease affect you and your family?

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Why the dengue situation in Pakistan could be a looming disaster…

“Dengue is now endemic in Pakistan…” said Dr. Muhammad Uzair Mukhtar from the Laboratory of Vector and Vector-Borne Disease at the Chinese Academy of Agricultural Sciences in Beijing. “It has been for the last ten years.” In an interview with Break Dengue, we explored the history of dengue in Pakistan, and he shared his most recent research and insights on what needs to be done to reduce the impact of this disease in the country.

What is the current status of dengue in Pakistan?

The first documented outbreaks of dengue in Pakistan were in 1994 in Karachi, when used tires imported from Thailand were the suspected source of the infection. But if you go back to the 1960s, there was one unconfirmed case of dengue in Pakistan.

Between 1994 and 2016 there were 71,649 cases with 797 deaths. 2010 was the worse year with almost 500 deaths in Karachi and Lahore. That year we had abnormal rainfall and flooding, compounded by people migrating from the cities to suburban areas.

Overall, the DENV2 dengue serotype is spreading across Pakistan – the same serotype detected in Karachi in 1994. Outbreaks started in the coastal region (including Karachi), then shifted to the lowland plains in 2011 (including Lahore) and to the highlands where there was a severe outbreak with deaths in Swat in 2013. Dengue shifted to cities in northern areas in 2017, where a severe outbreak led to 70 deaths. Only the arid region (the southeastern desert along with southwestern Balochistan) has not yet reported dengue.

What are the primary risk factors for dengue?

Recently, we studied the prevalence of dengue in Multan, located south of Punjab, to better understand the disease transmission dynamics and population at risk. It was Multan’s first dengue outbreak, and there were almost 1,000 cases of the disease recorded. Our data came from the Nishtar Hospital, where there were 689 suspected dengue patients – 373 confirmed.

The research concluded that around 11% of cases occurred during the rainy monsoon season (which runs from July to October) and the remainder in the months after – with no cases during the dry season. It also found most of those affected were aged between 21 and 49, and male. Our advice is that males should cover up, wear full-length sleeves as females do, and use insect repellent during the peak dengue season.

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We shared these recommendations with the health authorities during our routine case meetings. But Pakistan also needs to act to reduce mosquito populations before outbreaks occur – and embed these ideas in the minds of its people.

What would you like to see change?

In another study connected to dengue activity in Rawalpindi, we concluded that increased urbanization, insufficient water supply and inefficient removal of urban trash led to more non-biodegradable containers around human dwellings. These offered ideal breeding habitats for Aedes aegypti, which prefer roof-top water tanks and evaporative room coolers, followed by discarded tires and urban trash.

Image showing an unprotected team fogging in Pakistan.

“SOPs are not working well.” An unprotected team fogging in Pakistan. Image courtesy of Dr. Uzair

Bearing these findings in mind, we want governments and communities to remember vector control even after the peak dengue season. And we would like to see a shift towards Integrated Vector Management (IVM) designed to optimize the use of resources for effective vector control that is also cost-effective. IVM encompasses capacity building, inter-sector collaborations, an integrated approach, advocacy, and social mobilization, legislation, and evidence-based decision-making.

Pakistan already has advocacy initiatives through local governments, local representatives and the community, but it needs more public health education. And the standard operating procedures – for chemicals, for clothing, for dengue intervention – that are in place at a national and a provincial level are not working very well. On paper, they look good, but they are not fully implemented on the ground and are not providing the desired results.

Basically, there’s no permanent infrastructure for vector-borne diseases in Pakistan. Vector-borne disease control is a small section under the health department. When outbreaks happen, the dengue intervention begins – from inside a small section of the health department. It recruits untrained local people as field staff for dengue vector surveillance; the medical entomologists and the vector control experts needed are not there on a regular basis.

Do you have concerns regarding the current state of dengue control?

Vector control in Pakistan mainly involves chemical control using larvicides and adulticides. Temephos has been used as a larvicide in Pakistan since 1969. Everyone believed it was working well, with the larvae of the mosquito susceptible. But when we started looking into the insecticide susceptibility of Aedes aegypti and Aedes albopictus larvae in dengue-affected urban areas in Rawalpindi, we found mild resistance. Later, in 2016, a follow-up study confirmed emerging resistance of temephos in Aedes larvae in Rawalpindi.

For adulticides, a 2011 study reported a low level of resistance for DDT, malathion, and bendiocarb with the Malaria and dengue vectors. Five years later, we conducted the same study in Rawalpindi and found resistance for DDT, malathion, and bendiocarb, with mortality less than 90%. For deltamethrin and Lambda-cyhalothrin we found probable resistance present, with mortality was less than 97%.

With insecticides, the backbone of vector control in Pakistan, not having effective chemicals available in the future would be a disaster.

What’s needed to fortify dengue prevention in Pakistan?

The dengue situation in Pakistan is not good. It needs attention. After all, healthcare is critical to improving the daily lives of the people of Pakistan.

There is a lot of scope for research into dengue in Pakistan, but we need more resources, we need funding, and we need technical support from developed countries. There is an urgent need for an institute in Pakistan that yields medical entomologists and provides facilities for qualitative research on dengue and other vector-borne diseases.

Regarding the economic burden of dengue in Pakistan, for instance, I plan to conduct Knowledge, Attitude, and Practices (KAP) studies, and in these, I will include socio-economic factors and demographic factors in the dengue endemic areas of Pakistan.

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