Malaria in Suriname: a New Era
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MALARIA IN SURINAME: A NEW ERA IMPACT OF MODIFIED INTERVENTION STRATEGIES ON ANOPHELES DARLINGI POPULATIONS AND MALARIA INCIDENCE HÉLÈNE HIWAT - VAN LAAR Malaria in Suriname: a New Era Impact of modified intervention strategies on Anopheles darlingi populations and malaria incidence HÉLÈNE HIWAT – VAN LAAR ThESIS COMMITTEE ThESIS SUPERVISORS Prof. Dr. Ir. W. Takken Personal Chair at the Laboratory of Entomology Wageningen University Prof. Dr. M. Dicke Professor of Entomology Wageningen University OTHER MEMBERS Prof. Dr. Ir. H.F.J. Savelkoul Wageningen University Prof. Dr. R.W. Sauerwein Radboud University Nijmegen Prof. Dr. Ir. C. Leeuwis Wageningen University Dr.Ir. E.-J. Scholte New Food and Consumer Product- Safety Authority, Wageningen This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology and Resource Conservation. Malaria in Suriname: a New Era Impact of modified intervention strategies on Anopheles darlingi populations and malaria incidence HÉLÈNE HIWAT – VAN LAAR ThESIS Submitted in fulfillment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr. M.J. Kropff, in the presence of the Thesis committee appointed by the Academic Board to be defended in public On Monday 21 November 2011 At 4 p.m. in the Aula Hiwat – Van Laar, H MALARIA IN SURINAME: A NEW ERA. - Impact of modified intervention strategies on Anopheles darlingi populations and malaria incidence. PhD Thesis, Wageningen University, Wageningen, NL (2011) With references, with summary in Dutch ISBN 978-94-6173-037-4 ABSTRACT Malaria is an infectious disease caused by Plasmodium blood parasites 5 | which live inside the human host and are spread by Anopheles mosquitoes. Every year an estimated 225 million new cases and near 800,000 malaria deaths are reported. Control of the disease is a formidable task involving all three living organisms (parasite, vector and host) and their environment. Human hosts are mobile and play an important role in the spread of the disease. Anopheles mosquitoes, also mobile, have a tendency to adapt to new environments and are able to counter-act control measures, for instance by developing insecticide resistance. Plasmodium parasites, highly adaptive, develop drug resistance, thus rendering existing malaria treatments useless. Finding new methods and strategies to control and eliminate malaria is a continuous struggle. Nowadays malaria control strategies contain a complex of measures complementing one another. New tools are being developed. In 2005 a new 5-year malaria program was initiated in Suriname which combined a number of old, improved and new malaria control measures and strategies. This thesis describes the effect of these measures and strategies on malaria incidence and the Anopheles darlingi populations in Suriname and also evaluates some mosquito monitoring tools. Suriname has been fighting malaria since the early 1900s. As in many other countries in Latin America, control efforts were successful in the 1950s and 1960s and Suriname succeeded in getting the coastal area free of malaria. In the interior, transmission continued and malaria incidence ABSTRACT increased. An important role in malaria transmission is played by the mosquito Anopheles darlingi, the primary vector in Suriname. This vector species is important throughout its distribution area in South America. It has a preference for human blood and is highly effective in transmitting malaria even when population densities are low. It combines these capacities with diverse behavioral characteristics and an ability to adapt to new situations, which make it a difficult vector to control. The density of host-seeking Anopheles mosquitoes is an important factor in determining malaria transmission risk. This density is traditionally assessed by collecting and counting the number of mosquitoes which land on a human collector in order to bite; the human landing collections. Most often the landing mosquitoes are collected before they bite, but obviously this method may hold a risk for the collectors when used in a malaria | 6 endemic area. Besides, it is a very labor-intensive and expensive method. Alternative tools are needed. The ability of the CDC Miniature light trap, the BG Sentinel™ trap and the Mosquito Magnet® Liberty Plus, with carbon dioxide or a protected human as bait, to act as an alternative to human landing collections in defining mosquito biting pressure was tested both for An. darlingi and Anopheles aquasalis. Even though in particular the BG Sentinel and the Mosquito Magnet Liberty Plus showed potential, none of the trapping methods proved as effective as the human landing collections. As it turns out carbon dioxide may not be a sufficient stand-alone bait for these Anopheles species. Alternative baits, especially human-derived stimuli, may improve the results, enabling a more cost-effective mosquito monitoring and surveillance tool, with less risks. The BG Sentinel trap, baited with CO₂, was very efficient in collecting Culex mosquitoes. The most important changes in the malaria control strategy in Suriname as of 2005 were 1) the introduction of artemisinin-based combination therapy as a new first line treatment for malaria caused by Plasmodium falciparum, just prior to the onset of the new malaria program, and 2) the mass-distribution of free long-lasting insecticide-treated nets (LLINs) to the population at risk. Other measures included Indoor Residual Spraying, Active Case Detection and training of on-site Malaria Service Deliverers in remote areas. The effect of the control program on the mosquito populations was assessed in a 4-year longitudinal vector study in three sentinel sites, using human landing collections. Anopheles darlingi populations collapsed shortly after onset of the malaria control program and did not recover during the ABSTRACT following years. The possible impact of the LLINs on the mosquito population is discussed. Our limited knowledge about the reasons for the vector populations’ collapse and about An. darlingi ecology in general, prevent us from making predictions about future population dynamics. An. darlingi population densities remain low in the sentinel sites but a density increase could be triggered at any time. A continued monitoring of the vector and further studies with regard to its feeding behavior and ecology in general will therefore be necessary. The new malaria control strategy led to a significant decrease of malaria in the villages in the interior of the country, enabling Suriname to reach the Millennium Development Goal for malaria in 2007. The malaria situation in Suriname changed to a state where the disease is almost completely controlled in the stabile populations of the villages in the interior where malaria incidence is down to near elimination levels. This is a significant 7 | success, but can Suriname hold on to it? Transmission still occurs in the mobile human populations in the forest, especially among the gold miners. Additionally, the border region with French Guiana is vulnerable due to cross-border movement of the people. The new challenge for Suriname is to further control and possibly (locally) eliminate malaria by establishing an integrated malaria control strategy with a strong malaria surveillance system and prompt interventions in areas of renewed outbreaks. This will require sufficient funds, dedication and regional collaboration. | 8 TABLE OF CONTENTS table of contents ABSTRACT 5 CHAPTER 1 General introduction 11 CHAPTER 2 Ecology of Anopheles darlingi with respect to vector importance: a review 21 CHAPTER 3 Evaluation of Methods for Sampling the Malaria Vector Anopheles darlingi in Suriname and the Relation with its Biting Behavior 41 CHAPTER 4 Studies with carbon dioxide baited traps as alternative for human landing collections of Anopheles 9 | aquasalis in Suriname 55 CHAPTER 5 Behavioral heterogeneity of An darlingi and malaria transmission dynamics along the Maroni river (Suriname, French Guiana) 63 CHAPTER 6 Collapse of Anopheles darlingi populations in Suriname after introduction of insecticide-treated nets (ITNs); malaria down to near elimination level 77 CHAPTER 7 Novel strategies lead to near elimination of malaria in previously high-risk areas in Suriname, South America 91 CHAPTER 8 Summarizing discussion 111 ABBREViaTIONS 120 REFERENCES 121 SaMENVATTING (DUTCH SUMMARY) 143 ACKNOWLEDGMENTS 147 CURRICULUM ViTAE 149 LiST OF PUBLICATIONS 151 PE&RC EdUCATION STATEMENT 153 | 10 CHAPTER 1 General Introduction 1 MALARIA IN SURINAME 11 | Malaria has had a profound impact on the history of Suriname. It resulted in the death of numerous Amerindians after the import of the so- called malaria tropica, caused by Plasmodium falciparum, as a result of the introduction of African slaves in colonial times (16th and 17th century). Other malaria species in Suriname are P. vivax and P. malariae. Malaria forced the European colonists to make a treaty with runaway slaves in the forest of the interior in 1760, because malaria among the troops prevented them from getting these slaves back and return them to forced labor. It seriously hampered the development of gold, timber and balata industries and cost the lives of hundreds of contractors from overseas working on the railroad going from the capital to the interior in the early 1900s (Van der Kuyp, 1969). This mostly happened before the discovery by Charles Laveran in 1880 of the Plasmodium blood parasites which cause malaria and before