Course:CONS200/2023WT1/Genetically modified mosquitoes as a tool to curb blood-borne diseases

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Anopheles mosquito

Mosquitoes have always been known as troublesome insects, due to the itchy bites they leave after feeding on human flesh with their proboscises[1]. However, they are also known for the variety of dangerous diseases they carry[1] that kill hundreds of thousands of people every year[2], the most known being the Anopheles mosquito that carries malaria. Recently, scientists have been testing out genetically modified mosquitoes as a tool for biological control in order to lessen the devastating effects of these diseases[3].

Although mosquitoes are seen as dangerous and troublesome[1], they have an important ecological role in their ecosystems[4]. There are 3500 named species of mosquito, of which only a couple hundred bite humans[4]. They live on almost every continent and habitat, and play a large part in food webs[4]. Many species of fish, insects, spiders, lizards, salamanders, and frogs use mosquitoes as their primary food source[4]. If mosquitoes were to be eradicated, some of these species would lose their primary food source, and potentially face extinction[4]. Mosquitoes are also important pollinators[4]. Mosquitoes pollinate thousands of plant species, as most adults depend on nectar as a food source - only females of some species need blood to obtain the necessary proteins to lay eggs[4]. Even though mosquitoes have important ecological roles, many scientists argue for their eradication[4]. The gaps they would leave in ecosystems would most likely be quickly filled by other insects, and there would be a significant reduction in the diseases they transmit[4]. However, scientists struggle with mechanisms for mosquito eradication, which makes this unlikely to occur[4]. Instead, scientists are now trying to genetically modify mosquitoes to be unable to carry these deadly diseases and release them into the wild as a way of reducing the harmful and destructive impacts of mosquito-borne diseases[3].

Impact of Mosquito-Borne Diseases

Mosquitoes (Culicidae) are vectors of a variety of pathogens capable of causing life-threatening disease in humans such as malaria, yellow fever, and many forms of infectious encephalitis[5]. It is estimated that one billion people annually are infected by mosquito-transmitted diseases, resulting in over a million deaths worldwide[6]. Plasmodium alone is estimated to cause half a million malaria-related deaths in sub-Saharan Africa annually[7]. Along with the loss of human life, the cost of treating patients with malaria costs an estimated twelve billion USD per year, with the true economic losses many times greater when productivity loss is accounted for[8]. For example, the 2005 outbreak of West Nile virus in California resulted in 163 human cases amounted to nearly 3 million dollars in economic losses, with an estimated 1.6 million being productivity loss[9].

Photo of a ʻIʻiwi taken by a U.S. Fish and Wildlife Service employee[10]

Vector-borne diseases also have a negative impact on vulnerable wildlife populations[11]. Introduced southern house mosquitoes (Culex quinquefasciatus) is the main vector of avian malaria (Plasmodium relictum) and the avian pox virus (Avipoxvirus), two major drivers of the extinction of endemic bird species across the Hawaiian Islands[12]. Without adequate disease control, the diseases are projected to greatly contribute to the extinction of all six remaining species of Hawaiian honeycreepers before the year 2033[13]. With only 95 of the 142 endemic bird Hawaiian bird species left, it is essential for measures to stop the negative impacts of mosquito borne diseases in order to protect these cultural and scientifically significant species[14]. For instance, the ʻIʻiwi (Drepanis coccinea), is an endemic species of honeycreeper experiencing significant population declines due to lacking immunity for both avian malaria or Avipoxvirus[15]. The bird is considered sacred to the Indigenous peoples of Hawaii and its feathers are often used to decorate clothing for ceremonies[15]. Feeding habits and bill shape of this group of finches (Fringillidae) is unique and not observed in another other group in its taxonomic family[16]. Honeycreepers are often used by researchers to study ecological processes such as niche partitioning and adaptive radiation[16].

Disease Control Using Genetic Modification

The use of genetically modified mosquitoes aims to reduce the transmission of blood-borne illnesses by replacing disease carrying mosquitoes with ones that cannot carry the diseases or simply suppress the mosquito population altogether[17]. In the case of producing genetically modified mosquitoes that cannot carry blood-borne diseases, or population transformation, a successful approach developed at the University of California Irvine began by analyzing malaria antibodies in mice, then developed genes that could produces the same antibodies in the Anopheles stephensi mosquito, and finally the modified genes were implanted into the mosquitoes using CRISPR technology[18]. Researchers found that when exposed to malaria, these modified mosquitoes completely eliminated the disease; moreover, an additional advantage of this method is that it can be easily applied to other species of mosquitoes with little effort[18]. Once the genetically modified mosquitoes mate, the malaria blocking gene is passed onto 99.5% of offsprings, allowing the gene to be passed on automatically from generation after generation[19].

On the other hand, biotechnology company Oxitec produced genetically modified mosquitoes whose offsprings would die prior to maturity using a method called "Release of Insects carrying a Dominant Lethal", or mosquitoes carrying a lethal gene that prevents them from reaching maturity, allowing for mosquito population suppression[20]. Modified mosquitoes are raised to maturity in a lab using tetracycline, which inhibits the lethal gene that prevents the mosquitos from reaching maturity, then only the male modified mosquitoes are released to the environment to mate with wild females to produce non-viable larve as they cannot survive without the presence of tetracycline, thus suppressing the wild mosquito population[20]. Females are not released due to public concerns over genetically modified mosquito bites as only female mosquitos bite for nutrition to produce offspring[21].

Comparing the effectiveness two types of genetically modified mosquitoes against blood-borne illnesses such as malaria, both methods are viable solutions for the problem, however the modified mosquito for population transformation allows for effective disease control with a singular release, given that the modified gene is successfully passed on to wild mosquitoes[22]. This offers a low cost and maintenance solution compared to mosquito population suppression, as the genetically modified mosquitoes with the lethal gene do not successfully reproduce outside of a lab environment, thus requiring the constant production and release of modified mosquitoes for continual disease control and mosquito suppression[22].

Barriers to the Development of Genetically Modified Mosquitoes

Although disease-free mosquitoes have already been developed in many laboratory trials, current results have failed to yield organisms that can outcompete with wild populations[3]. Another issue researchers face is that many mosquito borne diseases use multiple species to transmit between hosts[3]. Malaria alone has around 70 vectors, making the task of developing a genetically modified population of each species that can also outcompete existing populations difficult and costly[3]. Mosquitoes are also incapable of respecting political boundaries where conflicts between governments may arise due to different policies regarding genetically modified organisms[3]. This has already started to become an issue with genetically modified crops in the United States, primarily caused by ineffective legislation and an inability to detect escapees before they are established in a new environment[18]. Although many of the long-term impacts of escaped genetically modified organisms are unknown due to a lack of research time, they have the potential to become pests shall they escape into other jurisdictions or from a lack of regulation[18].

Concerns have been raised about a possible lack of trust from communities regarding white scientists releasing a lab created organism into the homes of people living in less developed countries that has a potential to have a huge control over their lives[17]. Historical and on-going injustices regarding minority representation and treatment in areas in the scientific community has understandably resulted in a level of mistrust towards researchers, making data collection more difficult [23].

Additionally, there is little known about how these modified mosquitoes interact with the environment by hybridizing with other species and if it would have adverse effects on the ecosystem[24]. This can affect the genetic diversity of wild populations and may result in the loss of genes associated with isolated populations of mosquitoes that make them unique[25]. Even if GMO mosquitoes are unable to interbreed with existing populations, there exists a moral debate on the useable of genetic modification[26]. For instance, in order for genetically modified mosquitoes to be effective, it requires them to outcompete existing populations[3]. Some people believe that replacing existing populations of with GMOs may have unintended consequences on the ecosystem [27].

Examples of Genetically Modified Mosquitoes in Use

Brazil, starting in 2011 Brazil release 10 million of GM mosquitoes to reduce the population of Aedes aegypti mosquitoes carrying dengue[28]. During 2013-2015 Oxitec released 450,00 mosquitoes per week[29]. Oxitec reports that OX513A has reduced the wild mosquito population from 80-95% with their extension claiming to have reduced the risk of Dengue. Mosquitoes are still prevalent because of poor urbanization structure, inadequate water supply's and unreliable sanitation[30]

The Grand Cayman, in 2010, Oxitec initiated a partnership with the Cayman Islands, investing $588,000 into a project designed to tackle specific challenges. However, the collaboration ceased in December 2017 due to the project's outcomes falling short of initial expectations. Despite efforts and investment, the anticipated effectiveness wasn't achieved, leading to the conclusion of the venture between Oxitec and the Cayman Islands.[31]

Panama, In 2014, Oxitec initiated a groundbreaking campaign in Panama by releasing its first batch of genetically modified (GM) mosquitoes as part of the fight against dengue fever. This pivotal step marked the company's concerted effort to combat the disease by employing innovative genetic modifications. Furthermore, Oxitec's commitment extended beyond dengue fever, as evidenced by its parallel malaria program operating in Djibouti and Panama. Notably, this malaria program received substantial backing in the form of an $18 million grant from the Bill & Melinda Gates Foundation, signifying a significant investment in the pursuit of advanced solutions to tackle mosquito-borne illnesses.

In India, the urgent need to address the severe impact of Aedes aegypti, responsible for infecting approximately 5.8 million people annually, has led Gangabishan Bhikulal Investment and Trading Ltd to explore Oxitec's genetically sterile mosquitoes[32]. The company aims to showcase the efficacy of these modified mosquitoes in suppressing the local Aedes aegypti population. This move becomes crucial given the resistance observed due to the inefficacy of other genetically modified plants. The hope rests on Oxitec's innovative approach to combat this mosquito-borne menace, which poses a significant health threat across the country.[33]

Advantages of Alternative Mosquito Control Methods

Traditional mosquito-borne disease control methods involve the use of residual insecticides on mosquito nets or through fogging[34], as well as the larval control through the elimination of breeding sites[35]. Insecticide use to control mosquitoes offers several advantages to genetically modified mosquitoes: widespread availability, low cost and known impacts on the environment[34]. Additionally, insectide use is a mature method of vector-borne illness control used in at least 143 countries, representing 97% of the global population, and the affordability of insecticides allows it to be used in both developed and developing countries[36], unlike genetically modified mosquitoes, which have only been tested in parts of Brazil, the Cayman Islands, Panama, and India[37]. The impacts of insecticide use have also been well studied, while insecticides such as bifenthrin, deltamethrin, and permethrin are all highly toxic to pollinator species like bees[34], enviromental impacts from genetically modified mosquitos raise more profound concerns: the new genes introduced to genetically modified mosquitoes may transfer to other species through the process of horizontal transfer, causing permenent change to other species' genetic code such as sterilization[38].

Larval control through the elimination of breeding sites has been extremely successful in Southeast Asia, Europe and the Americas[35]. Mosquitoes only breed in standing water, therefore the draining of puddles and swamps near populated areas would greatly reduce a source of disease carrying mosquitoes[39]. The elimination of breeding sites creates minimal impacts to the environment compared to pesticide use and novel bio-engineered entities, and is nearly management-free with adequate drainage to prevent water from pooling up once more[39].

Ethical and Environmental Concerns

While genetically modified mosquitoes present an innovative possibility for biological control[3], they present some ethical and environmental concerns[40]. One of the most important ethical concerns is obtaining the support of the community in which field trials are conducted[41]. Researchers cannot legally conduct experiments in most countries without first obtaining the approval of national and local authorities[41]. While that mostly includes legal requirements, it also includes ethical requirements[41]. Ethics, guided by the principles of autonomy and justice[41], require that the people who are most likely to be impacted by field trial or research project should be able to voice their opinions about and have input into the decision-making related to the project[41].

However, this presents many challenges. In field trials that extend over large areas, it is not possible to obtain consent from each individual community member[41]. Because of this, researchers aim to obtain community consent and need to develop a strong community engagement strategy that meets approved standards of the affected population[41]. This can also be difficult because large parts of the community often have concerns and skepticisms surrounding the release of genetically modified mosquitoes[41]. For example, following a 2010 dengue fever outbreak in Key West, Florida, the Florida Keys Mosquito Control District announced that they were considering a proposal to release GM mosquitoes[41]. Public perceptions that were initially positive began to change as many of the residents in the targeted county (Key Haven) expressed concerns about the potential public health and environmental risks, some going as far as to start petitions and circulate letters[41]. Eventually, the residents of Key Haven voted against the proposal but the county as a whole voted in favour. This means that the trials will have to take place in a different part of the county[41]. This is a good example of how community consent is important and necessary if field trials are to be conducted in an ethical manner[41].

In addition to ethical concerns, there are also significant ecological challenges concerning the use of genetically modified mosquitoes[42], mainly due to the uncertainty of this new technology and the absence of research surrounding their possible impact not only on the environment and but on humans as well. There are concerns about how they could negatively impact non-target organisms and species diversity due to gene transfer and their effects on the ecosystem[40]. There are also concerns about the emergence of new diseases or possible negative impacts on human health[40].

While there are concerns, there are regulations and agreements for this exact reason, such as The Cartagena Protocol on Biosafety to the Convention on Biological Diversity, which is an international agreement that ensures the safe handling, transport, and use of living modified organisms [43]. This protocol takes into account potential effects on biological diversity and risks to human health[43].

Conclusion

While mosquitoes are dangerous insects that pose a threat to humans due to the dangerous diseases they transmit[44], they can be used as a tool to help prevent the spread of these diseases by genetically modifying them[45]. Mosquito-borne diseases infect an estimated one billion people per year[46] and also have a negative impact on wildlife populations[47]. Genetically modified mosquitoes aim to replace the disease carrying mosquitoes with mosquitoes that are not able to carry these diseases through genetic modification[48]. Disease-free mosquitoes have been developed in many lab trials, but they face challenges in field trials because the genetically modified mosquitoes fail to outcompete with natural mosquitoes[45], and communities lack the trust of the scientists who created these mosquitoes due to their unknown nature[48]. There are other methods of reducing mosquito populations, including mosquito nets, fogging[49], and many different insecticides[50]. There are also some ethical and environmental concerns surrounding field trials of genetically modified mosquitoes, like obtaining the consent of the communities in which these field trials will take place[51], and the impacts on the surrounding ecosystems[52]. Genetically modified mosquitoes offer a new and innovative technique for disease control[45], however there are many challenges and concerns that must be dealt with before their successful usage[53].

References

  1. ↑ 1.0 1.1 1.2 Horsfall, W. E. (1955). "Mosquitoes. Their bionomics and relation to disease". Mosquitoes. Their Bionomics and Relation to Disease.
  2. ↑ Ngwa, G. A. (2000). "A mathematical model for endemic malaria with variable human and mosquito populations". Mathematical and computer modelling. 32(7-8): 747–763.
  3. ↑ 3.0 3.1 3.2 3.3 3.4 3.5 3.6 3.7 Beisel, Uli; Boëte, Christophe (April 8, 2013). "The Flying Public Health Tool: Genetically Modified Mosquitoes and Malaria Control". Science as Culture. 22(1): 38–60 – via Taylor & Francis Online.
  4. ↑ 4.0 4.1 4.2 4.3 4.4 4.5 4.6 4.7 4.8 4.9 Fang, Janet (21 July 2010). "Ecology: A world without mosquitoes". Nature. 466: 432–434 – via Nature.
  5. ↑ CDC (March 21, 2016). "mosquito-borne diseases".
  6. ↑ Omodior, Oghenekaro; Luetke, Maya; Nelson, Erik (December, 2018). "Mosquito-borne infectious disease, risk-perceptions, and personal protective behavior among U.S. international travelers". Preventive Medicine Reports. 12: 336–342 – via Science Direct. Check date values in: |date= (help)
  7. ↑ Cheshire, William (Spring 2018). "If mosquitoes were to disappear from the world". Health and Medicine. 34 (1) – via Gale OneFile.
  8. ↑ CDC (December 16, 2021). "Malaria's impact worldwide".
  9. ↑ Barber, Loren; Schleier, Jerome; Peterson, Robert (March, 2010). "Economic cost analysis of West Nile Virus outbreak, Sacramento County, California, USA, 2005". Emerging Infectious Diseases. CDC. 16 (3): 480–486. Check date values in: |date= (help)
  10. ↑ U.S. Fish and Wildlife Service (January 28, 2006). "Iiwi". Wikimedia Commons.
  11. ↑ Stuchin, Margot; Machalaba, Catherine; Karesh, William (September 21, 2016). "Vector-borne diseases: animals and patterns". National Academies Press.
  12. ↑ Samuel, Michael; Woodworth, Bethany; Atkinson, Carter; Hart, Patrick; LaPointe, Dennis (June 30, 2015). "Avian malaria in Hawaiian forest birds: infection and population impacts across species and elevations". Ecosphere. 6 (6): 1–21 – via Ecological Society of America.
  13. ↑ Green, Josh; Chang, Dawn (March 25, 2023). "Endangered forest birds to receive protection from avian malaria on Maui". Government of Hawaii.
  14. ↑ American Bird Conservancy (n.d.). "Paradise for some–but an ongoing extinction crisis for birds".
  15. ↑ 15.0 15.1 American Bird Conservancy (n.d.). "ʻIʻiwi".
  16. ↑ 16.0 16.1 Tokita, Masayoshi; Yano, Wataru; James, Helen; Abzhanov, Arhat (February 5, 2017). "Cranial shape evolution in adaptive radiations of birds: comparative morphometrics of Darwin's finches and Hawaiian honeycreepers". Biological Sciences. 372 (1713) – via The Royal Society.
  17. ↑ 17.0 17.1 Jones, Sam (June 28, 2023). "How genetically modified mosquitoes could eradicate malaria". Nature.
  18. ↑ 18.0 18.1 18.2 18.3 Vasich, Tom. "New breed of mosquitoes can't transmit malaria". University of California. Cite error: Invalid <ref> tag; name ":9" defined multiple times with different content
  19. ↑ Gantz, Valentino; Jasinskiene, Nijole; Tatarenkova, Olga. "Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi". Proceedings of the National Academy of Sciences. 112.
  20. ↑ 20.0 20.1 Schairer, Cynthia; Najera, James; James, Anthony. "Oxitec and Mosquitomate in the United States: Lessons for the future of Gene Drive Mosquito Control". Pathogens and Global Health. 115: 365–376.
  21. ↑ Environmental Protection Agency. "Following Review of Available Data and Public Comments, EPA Expands and Extends Testing of Genetically Engineered Mosquitoes to Reduce Mosquito Populations". United States Environmental Protection Agency.
  22. ↑ 22.0 22.1 Reis-Castro, Luísa (December 2012). "Genetically modified insects as a public health tool: Discussing the different bio-objectification within genetic strategies". Croatian Medical Journal. 53: 635–638.
  23. ↑ Funk, Carey; Lopez, Mark (June 14, 2022). "3. Hispanic Americans' trust in medical scientists and views about the potential for researcher misconduct". Hispanic Americans' Trust in and Engagement With Science – via Pew Research Centre.
  24. ↑ Resnik, David (December 21, 2012). "Ethical issues in field trials of genetically modified disease-resistant mosquitoes". Developing World Bioethics. Wiley Online Library. 14 (1): 37–46.
  25. ↑ Landry, Heather (August 10, 2015). "Challenging evolution: how GMOs can influence genetic diversity". Harvard University.
  26. ↑ Weale, Albert (November 30, 2010). "Ethical arguments relevant to the use of GM crops". New Biotechnology. 27 (5): 582–587 – via Science Direct.
  27. ↑ Schwindenhammer, Sandra (January 16, 2020). "The rise, regulation and risks of genetically modified insect technology in global agriculture". https://journals.sagepub.com/doi/10.1177/0971721819890042. 25 (1) – via Sage Journals. External link in |journal= (help)
  28. ↑ Waltz, Emily (March 2016). "Gm mosquitoes fire first salvo against Zika virus". Gale Onefile. Retrieved 30/11/23. Check date values in: |access-date= (help)
  29. ↑ Servick, Kelly (20/09/2019). "GM mosquito study draws fire". Science. Retrieved 12/12/2023. Check date values in: |access-date=, |date= (help)
  30. ↑ Araujo, Helena; Carvalho, Danilo; Loshino, Rafaella; Costa-da-Silva, Andre; Capurro, Margareth (11/6/2015). "Aedes aegypti Control Strategies in Brazil: Incorporation of New Technologies to Overcome the Persistence of Dengue Epidemics". MDPI. Retrieved 13/12/2023. Check date values in: |access-date=, |date= (help)
  31. ↑ Whittaker, James (04/12/2018). "Cayman Islands Abandons Failed GM Mosquito Project". Biosafety Information Centre. Retrieved 29/11/2023. Check date values in: |access-date=, |date= (help)
  32. ↑ Noisette, Christophe (October 3 2023). "GMO mosquitoes : Oxitec comes back to Panama". inf’OGM. Retrieved December 13 2023. Check date values in: |access-date=, |date= (help)
  33. ↑ Wadke, Rahul (August 20 2018). "Govt may swat GM mosquitoes". ProQuest. Retrieved December 1 2023. Check date values in: |access-date=, |date= (help)
  34. ↑ 34.0 34.1 34.2 World Health Organization (2004). "Global Strategic Framework for Integrated Vector Management". World Health Organization.
  35. ↑ 35.0 35.1 Centers for Disease Control and Prevention (July 16, 2020). "Larval Control and Other Vector Control Interventions". Centers for Disease Control and Prevention.
  36. ↑ Van den Berg, Henk (2012). "Global trends in the use of insecticides to control vector-borne diseases". Environmental Health Perspectives. 120: 577–582.
  37. ↑ Centers for Disease Control and Prevention (July 2022). "Genetically Modified Mosquitoes". Centers for Disease Control and Prevention.
  38. ↑ House of Parliament Office of Science and Technology (June 2010). "Genetically Modified Insects" (PDF). UK Parliament.
  39. ↑ 39.0 39.1 Government of Ontrario (May 2022). "Controlling mosquitoes on rural and farm properties". Ministry of Agriculture, Food and Rural Affairs.
  40. ↑ 40.0 40.1 40.2 Hartley, Sarah (Mar 16, 2021). [10.1186/s12936-021-03682-6 "Ugandan stakeholder hopes and concerns about gene drive mosquitoes for malaria control: new directions for gene drive risk governance"] Check |url= value (help). Malaria journal – via PubMed Central.
  41. ↑ 41.00 41.01 41.02 41.03 41.04 41.05 41.06 41.07 41.08 41.09 41.10 41.11 Resnik, David B. (May 3, 2017). "Ethics of community engagement in field trials of genetically modified mosquitoes". Developing world bioethics. 14(1): 37–46 – via Wiley Online Library.
  42. ↑ Knols, Bart G.J. (2003). Ecological Aspects for Application of Genetically Modified Mosquitoes. Springer Science & Business Media. pp. 235–242.
  43. ↑ 43.0 43.1 Ostera, Graciela R. (2011). "Biosafety concerns involving genetically modified mosquitoes to combat malaria and dengue in developing countries". JAMA. 305(9): 930–931 – via JAMA.
  44. ↑ Horsfall, W. E. (1955). "Mosquitoes. Their bionomics and relation to disease". Mosquitoes. Their Bionomics and Relation to Disease.
  45. ↑ 45.0 45.1 45.2 Beisel, Uli; Boëte, Christophe (April 8, 2013). "The Flying Public Health Tool: Genetically Modified Mosquitoes and Malaria Control". Science as Culture. 22(1): 38–60 – via Taylor & Francis Online.
  46. ↑ Omodior, Oghenekaro; Luetke, Maya; Nelson, Erik (December, 2018). "Mosquito-borne infectious disease, risk-perceptions, and personal protective behavior among U.S. international travelers". Preventive Medicine Reports. 12: 336–342 – via Science Direct. Check date values in: |date= (help)
  47. ↑ Stuchin, Margot; Machalaba, Catherine; Karesh, William (September 21, 2016). "Vector-borne diseases: animals and patterns". National Academies Press.
  48. ↑ 48.0 48.1 Jones, Sam (June 28, 2023). "How genetically modified mosquitoes could eradicate malaria". Nature.
  49. ↑ World Health Organization (2004). "Global Strategic Framework for Integrated Vector Management". World Health Organization.
  50. ↑ Van den Berg, Henk (2012). "Global trends in the use of insecticides to control vector-borne diseases". Environmental Health Perspectives. 120: 577–582.
  51. ↑ Resnik, David B. (May 3, 2017). "Ethics of community engagement in field trials of genetically modified mosquitoes". Developing world bioethics. 14(1): 37–46 – via Wiley Online Library.
  52. ↑ Knols, Bart G.J. (2003). Ecological Aspects for Application of Genetically Modified Mosquitoes. Springer Science & Business Media. pp. 235–242.
  53. ↑ Hartley, Sarah (Mar 16, 2021). [10.1186/s12936-021-03682-6 "Ugandan stakeholder hopes and concerns about gene drive mosquitoes for malaria control: new directions for gene drive risk governance"] Check |url= value (help). Malaria journal – via PubMed Central.


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