Review Article
Current Concepts
Control of Neglected Tropical Diseases
N Engl J Med 2007; 357:1018-1027September 6, 2007
- Article
The neglected tropical diseases are a group of 13 major disabling conditions that are among the most common chronic infections in the world's poorest people. A blueprint for the control or elimination of the seven most prevalent neglected tropical diseases — ascariasis, trichuriasis, hookworm infection, schistosomiasis, lymphatic filariasis, trachoma, and onchocerciasis — has been established by a group of private, public, and international organizations working together with pharmaceutical partners and national ministries of health. Through the newly established Global Network for Neglected Tropical Diseases, with updated guidelines for drug administration issued by the World Health Organization (WHO), partnerships are coordinating their activities in order to launch a more integrated assault on these conditions. If new resources are made available, as recommended by the Commission for Africa, a scaled-up approach to simple interventions could lead to sustainable decreases in poverty in some of the world's poorest countries. These decreases would represent a major success story for the United Nations Millennium Declaration.
“Other Diseases”
The Millennium Declaration, adopted by world leaders at the United Nations in September 2000, establishes an ambitious set of eight millennium development goals to eliminate extreme poverty, hunger, and disease by 2015. The sixth goal, “to combat HIV–AIDS [human immunodeficiency virus infection–acquired immunodeficiency syndrome], malaria, and other diseases,” specifically addresses the health and economic impact of infectious diseases. This goal has led to considerable and welcomed large-scale financial support through ambitious initiatives sponsored by the Group of Eight (G8) governments to fight HIV–AIDS and malaria. These initiatives include the U.S. President's Emergency Plan for AIDS Relief, the U.S. President's Malaria Initiative, and the Global Fund to Fight AIDS, Tuberculosis, and Malaria.1-5 However, programs to combat many of the “other diseases,” particularly the neglected tropical diseases, have not yet benefited from such support.1-5
The 13 parasitic and bacterial infections known as the neglected tropical diseases include three soil-transmitted helminth infections (ascariasis, hookworm infection, and trichuriasis), lymphatic filariasis, onchocerciasis, dracunculiasis, schistosomiasis, Chagas' disease, human African trypanosomiasis, leishmaniasis, Buruli ulcer, leprosy, and trachoma.2-4 An expanded list could include dengue fever, the treponematoses, leptospirosis, strongyloidiasis, foodborne trematodiases, neurocysticercosis, and scabies,4 as well as other tropical infections. The parasitic and bacterial diseases identified as being neglected are among some of the most common infections in the estimated 2.7 billion people who live on less than $2 per day. These diseases occur primarily in rural areas and in some poor urban settings of low-income countries in sub-Saharan Africa, Asia, and Latin America (Table 1Table 1
The Major Neglected Tropical Diseases Ranked by Prevalence.). The neglected tropical diseases lead to long-term disability and poverty.2-5,20 The poverty results from disfigurement or other sequelae of long-term illness, impaired childhood growth and development, adverse outcomes of pregnancy, and reduced productive capacity (Table 2Table 2
Major Characteristics of the Most Prevalent Neglected Tropical Diseases.).3,21,22 These features contrast with those of emerging acute infections, such avian influenza, Ebola virus infection, and West Nile virus infection.5 In aggregate, the neglected tropical diseases cause approximately 534,000 deaths annually.4 This substantial number of deaths is considerably less than that resulting from lower respiratory tract infections, diarrheal diseases, HIV–AIDS, or malaria. However, if metrics are applied to the disability and poverty associated with these diseases, the neglected tropical diseases can be shown to constitute large burdens on the health and economic development of low-income countries. In terms of disability-adjusted life-years, the neglected tropical diseases together rank closely with diarrheal diseases, ischemic heart disease, cerebrovascular diseases, malaria, and tuberculosis as being among the most important health problems in the developing world (Figure 1Figure 1
The 10 Leading Causes of Life-Years Lost to Disability and Premature Death.).4,5 In addition, the effect of the neglected tropical diseases on worker productivity causes annual losses of billions of dollars.24-27 Preventive Chemotherapy
Through the expanded use of mass drug administration as well as targeted treatments, we now have the opportunity to control or even eliminate some of the most important neglected tropical diseases in terms of prevalence and disease burden.1-5,20,28-39 The use of mass drug administration for the control of neglected tropical diseases, or preventive chemotherapy, was pioneered in China. In that country, the prolonged and targeted use of salt containing diethylcarbamazine resulted in the elimination of lymphatic filariasis as a public health problem,30 and the widespread use of praziquantel and other measures (including snail control and health education) is leading to the control of schistosomiasis.31 Egypt has also succeeded in reducing the prevalence of lymphatic filariasis and schistosomiasis and their associated morbidity.30,35
Such successes have laid a foundation for the establishment of international partnerships to control or eliminate these infections.1 A critical step occurred in the late 1980s, when Merck created the first partnership to control a neglected tropical disease; this partnership was formed to deliver donated ivermectin to treat onchocerciasis.3 To date, more than 300 million treatments have been provided, initially through the Onchocerciasis Control Program and subsequently through the African Programme for Onchocerciasis Control and the Onchocerciasis Elimination Program for the Americas.32 In addition, Pfizer has partnered with the International Trachoma Initiative to donate azithromycin as part of a comprehensive program to eliminate trachoma,33 and GlaxoSmithKline is working with the WHO, Merck, and the Global Alliance to Eliminate Lymphatic Filariasis to add donated albendazole to mass-drug-administration regimens of either diethylcarbamazine or ivermectin.34 These efforts have resulted in the near elimination of lymphatic filariasis as a public health problem in Egypt, Samoa, and Zanzibar30,34,35 and of trachoma as a public health problem in Morocco.36 Similarly, using donated generic formulations of praziquantel from MedPharm and other organizations, the Schistosomiasis Control Initiative and African health ministries have significantly reduced the disease burden of urinary and intestinal schistosomiasis in schoolchildren in six countries in East and West Africa,37,38 and the widespread use of albendazole and mebendazole is having an effect on school performance and the disease burden of soil-transmitted helminth infections,6 especially ascariasis and trichuriasis, among children. Dracunculiasis is on the verge of being eradicated.18,40,41 Many of these large-scale programs are being conducted in response to several World Health Assembly resolutions calling for the global control or elimination of the neglected tropical diseases with the greatest disease burden as a public health problem by the year 2020 or sooner.42,43
Integration of Control
Although great progress has been made in several countries,1-5,20,30-37 it is unclear whether existing financial resources and global political commitments are sufficient to reach the World Health Assembly's ambitious goals. Instead, it is likely that enhanced efforts will be required to expand global coverage and integrate measures to control the neglected tropical diseases. These efforts will involve harmonizing and coordinating the activities of the partnerships devoted to the control or elimination of the seven most prevalent neglected tropical diseases and linking them with national health ministries and the WHO. The rationale for integrating preventive chemotherapy measures is based on the observation that there is extensive geographic overlap and coendemicity among these seven diseases (Figure 2Figure 2
Nations with Five, Six, or Seven Neglected Tropical Diseases to Be Targeted for Integrated Preventive Chemotherapy.).2-5,20 Populations in such regions are infected with several different parasites and have multiple neglected tropical diseases simultaneously.2-5,20,46 Therefore, the delivery of a rapid-impact package of drugs is beneficial. The rapid-impact package is so named because the drugs can be quickly deployed by community-based distributors, with rapid reductions in disabilities, improvement in well-being, and, in some cases, interruption of disease transmission. This package includes a combination of four of six drugs: albendazole or mebendazole, praziquantel, ivermectin or diethylcarbamazine, and azithromycin.2 Through coordination of the partnerships to control neglected tropical disease and the public health infrastructures they create, these drugs can be delivered at an estimated cost savings of 26 to 47% as compared with nonintegrated programs.43 Because four of the six rapid-impact drugs are donated, the projected average total cost is as low as $0.40 to $0.79 per person per year in sub-Saharan Africa.2,43,47 Thus, an entire at-risk population of approximately 500 million could be treated for $400 million or less annually. Such estimates are a fraction of the annual costs of treatments with antiretroviral agents or directly observed multidrug therapy for tuberculosis.2 Moreover, the most prevalent neglected tropical diseases, especially hookworm infection and schistosomiasis, are frequently endemic with malaria and HIV–AIDS,4,48-51 and they have considerable coexisting or synergistic effects.49-51 Therefore, preventive chemotherapy could have an important collateral effect.4
To catalyze the integration of measures in order to control neglected tropical diseases, a group of partnerships that are committed to combatting the seven most prevalent of these diseases are cooperating with each other in the Global Network for Neglected Tropical Diseases. This network operates according to WHO treatment guidelines and algorithms and with vector management and other environmental control measures (Table 3Table 3
General Guidelines for Preventive Chemotherapy for the Seven Most Prevalent Neglected Tropical Diseases.).44 Integrated control of these diseases at the national level will require substantial financial resources to expand coverage of community-based mass drug administration and targeted treatments. The U.S. Agency for International Development recently announced a 5-year, $100 million award to provide preventive chemotherapy for 40 million people, and Geneva Global has committed $8.8 million for preventive chemotherapy in Rwanda and Burundi (Figure 2). The Bill and Melinda Gates Foundation has awarded $47 million to address critically important questions regarding operational research for effective integration. However, these awards constitute a fraction of the overall costs required to scale up programs in sub-Saharan Africa and elsewhere. It is estimated that a 5-year program to control or eliminate the major neglected tropical diseases in sub-Saharan Africa could cost approximately $1 billion to $2 billion. An estimated $2 to $9 per disability-adjusted life-year (i.e., per life-year lost to disability or premature death) would be averted for deworming,52 with up to 47% in cost savings through integration.43 This cost for the coordinated control or elimination of the seven most prevalent neglected tropical diseases represents a relatively inexpensive but potent public health intervention. It also represents a priority investment in human capital and a reduction in global poverty.53
The Need for New Tools of Control
Despite its enormous benefits, preventive chemotherapy with the rapid-impact package will not affect the three neglected tropical diseases with the highest rates of death — Chagas' disease, human African trypanosomiasis, and visceral leishmaniasis. Strategies to control these diseases are based on surveillance, early diagnosis and treatment, and vector control.17,54,55 These criteria for effective control present challenges because of the lack of appropriate diagnostic tools and safe drugs. To date, the greatest successes in the control of Chagas' disease and human African trypanosomiasis have occurred as a result of vector control. Vector control has dramatically reduced the transmission of Chagas' disease in five South American countries.54 The transmission of human African trypanosomiasis has been reduced through the use of simple, impregnated tsetse-fly traps that supplement surveillance and diagnostic measures.17
Although strategies to control and eliminate human African trypanosomiasis, leishmaniasis, and Chagas' disease are available,56,57 ultimately, success will almost certainly depend on access to new and cost-effective products for improved control. However, in the absence of commercial markets for drugs for neglected tropical diseases, the pipeline of new drugs for these diseases has virtually dried up during the past three decades.58 In response to this crisis, partnerships have been established to address product development for neglected tropical diseases. These partnerships for product development are either exploiting newly completed genome projects for protozoan parasites59 in order to identify potential drug targets for high-throughput screening or taking more traditional approaches to drug development and clinical testing.60 As a result of these activities, several new antiprotozoan drugs are under development for Chagas' disease, leishmaniasis, and human African trypanosomiasis, including miltefosine, paromomycin, sitamaquine, imiquimod, a pentamidine analogue known as DB289, and a vinyl sulfone known as K777, as well as combinations such as nifurtimox–eflornithine and paromomycin combined with antimonial agents.55,60-62 Highly efficacious drugs for the treatment of Buruli ulcer have not been developed.
Even with regard to the proposed rapid-impact package, challenges remain. These challenges include integrated and rapid mapping of the seven targeted diseases; careful assessment of safety, compatibility, and compliance; integrated monitoring and evaluation that are compatible with the capacity of the health system, on the one hand, and with scientific need, on the other; cost-effectiveness and cost–benefit studies; and analyses to determine the effect of integrated control on health systems.4,52 In countries such as Burkina Faso, Ghana, Niger, Nigeria, Togo, and Uganda, where integrated efforts to control neglected tropical diseases are under way, additional challenges have included limited access to drugs such as generic praziquantel (which is not yet donated on a large scale) and albendazole (which is currently donated only for the control of lymphatic filariasis), insufficient or fragmented funding, and a need for increased support from nongovernmental development organizations. In addition, African health ministries are beginning to struggle with the implementation of integrated control of neglected tropical diseases in the face of the demands of other disease-control programs, including G8-funded initiatives for HIV–AIDS, tuberculosis, and malaria. It is expected that these issues will pose particular challenges in areas that have experienced conflict and in fragile nation states.
Studies to determine the rates of post-treatment reinfection and to detect the emergence of anthelmintic drug resistance will be essential for monitoring and evaluation.4,5 The possibility that resistance has already emerged is a serious concern, especially for the benzimidazole anthelmintic agents (e.g., albendazole and mebendazole) and ivermectin,63,64 and without a new generation of tools for disease control and appropriate environmental control measures, the risk of repeating past mistakes remains.3,4,65 Therefore, it is important to commit resources to the improvement of available diagnostic tests and surveillance tools, especially for lymphatic filariasis and onchocerciasis,32,66 and to develop and test new, promising anthelmintic drugs such as tribendimidine for soil-transmitted helminth infections,67,68 a new macrofilaricide, and antiwolbachia-based therapies for the elimination of onchocerciasis.13 Although they are still experimental, medical therapies targeting wolbachia bacterial endosymbionts of filarial parasites offer new approaches to the reduction of parasite reproductive capacity and parasite-induced inflammation.69 However, the best prospect for the sustainable control of the neglected tropical diseases is the development of vaccines.21 Several vaccines against neglected tropical diseases, including vaccines against hookworm infection,68 schistosomiasis,70 and leishmaniasis,71 are in phase 1 and phase 2 clinical trials by partnerships for product development.4,21 In principle, it is possible to develop new “antipoverty vaccines” against all of the neglected tropical diseases21; these would be used as “vaccine-linked chemotherapy” alongside drugs in a comprehensive treatment and prevention framework.72
Drug and vaccine manufacturers from so-called innovative developing countries are assisting partnerships in their efforts to develop new products to control neglected tropical diseases. These middle-income countries, such as Brazil, China, and India, have the technical and industrial capacities to produce new drugs, vaccines, and diagnostic tests.3,73,74 Enhanced support by the G8 governments would accelerate innovation and essential health research for the developing world.75
Public Policy for Integrated Control
The High-Level Forum on the Health Millenium Development Goals has described partnership activities as best practices for moving forward a global agenda. Tackling neglected tropical diseases represents one of the “quickest wins” in terms of reducing the disease burden as well as developing new drugs and vaccines.2 There are additional opportunities to bundle the control of neglected tropical diseases with the control of malaria and HIV–AIDS.76 Such measures could exploit the geographic overlap of these conditions48 as well as potential synergies in public health control, with resultant cost savings.50,77 For example, a recent study showed that the administration of drugs for neglected tropical diseases by community distributors resulted in a ninefold increase in the distribution of antimalaria bed nets.77
Through partnerships to control the neglected tropical diseases and the Global Network for Neglected Tropical Diseases, a comprehensive framework is in place to provide preventive chemotherapy packages and to develop, test, and distribute a new generation of tools to control these diseases. This framework is an important model in disease control and poverty reduction. It also addresses important themes related to equity and ethics in developing countries78 and critical elements of humanitarian assistance; these themes could be incorporated into a larger foreign-policy framework.5 According to the United Nations Special Rapporteur on the right to the highest attainable standard of health, an effective and integrated program to control neglected tropical diseases strengthens local health systems, fosters community involvement in health, helps to ensure monitoring and accountability, and serves to destigmatize these conditions by dispelling myths and misconceptions about them through evidence-based information and education.78 The global community is now well positioned to control or eliminate neglected tropical diseases in developing countries and to link these efforts to programs to combat HIV–AIDS and malaria.
Dr. Hotez reports being director of the Human Hookworm Vaccine Initiative, which receives support from the Bill and Melinda Gates Foundation; an inventor on an international patent application (PCT/US02/33106) for hookworm vaccine; and president of the Sabin Vaccine Institute, which receives support from Geneva Global and support for activities unrelated to control of neglected tropical diseases from Merck, Wyeth, and GlaxoSmithKline. Dr. Molyneux reports being director of the Global Alliance to Eliminate Lymphatic Filariasis and the Lymphatic Filariasis Support Centre, which receives support from the United Kingdom Department for International Development and GlaxoSmithKline, and participating in the Mectizan Expert Committee/Albendazole Coordination meetings, which receive support from the Mectizan Donation Program supported by Merck. Dr. Fenwick reports being director of the Schistosomiasis Control Initiative, which receives support from the Bill and Melinda Gates Foundation. All of the authors except Dr. Savioli report being member partners of the Global Network for Neglected Tropical Diseases, which receives funding from Geneva Global. No other potential conflict of interest relevant to this article was reported.
Source Information
From the Sabin Vaccine Institute, and George Washington University, Washington, DC (P.J.H.); Liverpool School of Tropical Medicine Lymphatic Filariasis Support Centre and the Global Alliance to Eliminate Lymphatic Filariasis, Liverpool, United Kingdom (D.H.M.); the Schistosomiasis Control Initiative, Imperial College London, London (A.F.); the International Trachoma Initiative, New York (J.K.); the Earth Institute at Columbia University, New York (S.E.S., J.D.S.); and the Department of Neglected Tropical Diseases, World Health Organization, Geneva (L.S.).
Address reprint requests to Dr. Hotez at the Sabin Vaccine Institute and the Department of Microbiology, Immunology, and Tropical Medicine, George Washington University, Ross Hall 736, 2300 Eye St., NW, Washington, DC 20037, or at mtmpjh@gwumc.edu.
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