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Institute of Medicine (US) Forum on Microbial Threats. The Causes and Impacts of Neglected Tropical and Zoonotic Diseases: Opportunities for Integrated Intervention Strategies. Washington (DC): National Academies Press (US); 2011.

Cover of The Causes and Impacts of Neglected Tropical and Zoonotic Diseases

The Causes and Impacts of Neglected Tropical and Zoonotic Diseases: Opportunities for Integrated Intervention Strategies.

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A11PROGRESS IN CONTROL AND ELIMINATION OF HUMAN AFRICAN TRYPANOSOMIASIS, 201016

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World Health Organization

Background

Although quinine had been used by the French in Senegal since 1822 and given in 1844 to railroad workers in the United States as a prophylaxis, its prophylactic use was demonstrated by Baikie in 1854 in his Narrative of an Exploring Voyage up the Rivers Kwora and Binue. This evidence established that steamships could be taken up the Niger and Benue rivers and was instrumental in opening the interior to foreign commerce: missionary stations were established, and more than 250 miles of previously unexplored river (Binue) were explored and charted. No lives were lost to malaria as a result of pioneering prophylactic use of quinine. Baikie's stay on the river proved that Europeans from temperate zones could penetrate the interior and survive there. Thanks to this evidence, the Berlin treaty signed in 1885 allowed colonial countries to rush inside central Africa. A few years later, they had to face a new killer: human African trypanosomiasis (HAT), also known as sleeping sickness. The disease existed before the arrival of Europeans, but penetrating the continent and breaking into the environment were responsible for its dissemination.

One century ago, HAT was felt to curb the development of colonial territories. As soon as the cause of the disease was clearly identified at the beginning of the 20th century—and fearing an unpopulated continent and a shortage of human labour to exploit natural resources—colonial authorities decided to establish extensive control operations, with high levels of political commitment and strong involvement from eminent scientists such as Pasteur, Ehrlich, and Koch. Needed funds were allocated.

Large and intensive campaigns of systematic screening, treatment, and patient follow-up were established in West and Central Africa for the gambiense form of the disease, whereas animal reservoir and vector control was mainly implemented in east and south Africa for the rhodesiense form.

By the 1960s, transmission was practically interrupted in all endemic areas, providing evidence that the elimination of the disease was feasible and could be achieved with basic tools and strong committment. “It has become commonplace to say that trypanosomiasis is almost eradicated in Africa.… Although foci are relatively rare, they are nonetheless irritating” (Labusquière, 1965).

Thereafter, the rarity of cases led to a loss of interest for a sustained surveillance, and the risk of reemergence of the disease was overlooked. Thus, in the 1980s the disease reemerged. By the 1990s, flare-ups were observed throughout the past endemic areas, leading to a worrisome increase in the number of reported cases. Bilateral cooperation continued to support National Sleeping Sickness Control Programmes (NSSCPs) in some historically linked countries, but many areas or countries remained without any support or control activities. At this time, nongovernmental organizations (NGOs) played a crucial role in the control of HAT. However, their interventions were mainly focused on remote and insecure areas. As emergency operators, their policy understandably excluded the support to NSSCPs, which resulted in (1) the establishment of substitute HAT control systems, (2) the maintenance of a large part of the population at risk out of the umbrella of NGOs' projects, and (3) the difficulty for national programmes to sustain control achievements after NGOs' withdrawal.

The card agglutination trypanosomiasis test (CATT) for serological screening of HAT gambiense populations at risk was developed during the 1970s (Magnus et al., 1978), but its large-scale production encountered many problems that hindered its availability (Smith et al., 1998). Use of CATT was not widespread because NSSCPs could not afford to buy it. In addition, the production of anti-trypanosomal drugs was seriously threatened because of the lower economical return for manufacturers.

Research for new diagnostic tools and drugs was scarce (Stich et al., 2003). Only eflornithine, initially developed for cancer treatment, was finally registered for the treatment of the gambiense form of the disease, and only in 1990, without guarantee of being produced (Sjoerdsma and Schechter, 1999). Its cost, complex distribution, and administration made it inappropriate for the under-equipped peripheral health services in remote rural areas where HAT was prevalent. Only some well-funded NGOs were able to afford the cost of eflornithine treatment.

During the 1990s, security constraints due to civil wars and social upheavals complicated HAT control by preventing access to a large number of HAT-endemic areas, leading to difficulties in reaching a large number of affected populations and consequently to a considerable lack of epidemiological information. The World Health Organization (WHO) Expert Committee on HAT control and surveillance held in 1995, considering the huge uncertainties between the reported cases and the factual field situation, estimated that the true number of cases was at least 10 times more than reported. Thus, from the 30,000 cases reported annually, it was estimated that some 300,000 infected individuals remained ignored in the field (WHO, 1998).

In 1997, the 50th World Health Assembly expressed its concerns about the major recrudescence of cases by adopting a resolution to raise awareness and national and international interest (WHO, 1997). Subsequently, WHO enhanced its coordinating role and promoted networking with partners, developing a strong advocacy and awareness campaign. In 1999, a WHO treatment monitoring and drug resistance network was established with the collaboration of the Médecins sans Frontières (MSF) access campaign for essential drugs.

As a result, the private sector recognized its responsibility, which led Aventis Pharma to grant a substantial support to WHO in 2001 for the control and surveillance of HAT. This support included HAT drug donations and financial contributions, which allowed WHO to strengthen its support to disease-endemic countries (DECs). The establishment of this private–public collaboration marked the beginning of a new era in HAT control by expanding capacities for WHO control strategies. In 2002, Bayer Health Care began donating the last drug (suramin) to WHO.

The importance of the various components of the epidemiology of trypanosomiasis, (human, animal, vector control, agricultural activity, livestock production, etc.) and their impact on the development of rural Africa led WHO in 1995 to promote—together with the Food and Agriculture Organization (FAO), the International Atomic Energy Agency (IAEA) and the African Union Interafrican Bureau for Animal Resources (AU-IBAR)—an intersectoral initiative that, in 1997, ultimately became the Programme Against African Trypanosomiasis (PAAT).17

In parallel, during the African Union Summit in Lomé in 2000, the African heads of state and government established the Pan African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC)18 with the objective of rendering Africa a tsetse- and trypanosomiasis-free continent.

Current Situation

Between 2000 and 2009, out of 36 countries listed as endemic, 24 received the exclusive support of WHO either to assess the epidemiological status of HAT or to establish control and surveillance activities: Benin, Burkina Faso, Cameroon, Chad, Côte d'Ivoire, Gabon, Ghana, Guinea, Guinea Bissau, Kenya, Liberia, Malawi, Mali, Mozambique, Nigeria, Rwanda, Senegal, Sierra Leone, Swaziland, Togo, Uganda, United Republic of Tanzania, Zambia, and Zimbabwe; 6 received support from WHO as well as NGOs or through bilateral cooperation: Angola, Central African Republic (CAR), Congo, Democratic Republic of the Congo (DRC), Equatorial Guinea, and Sudan; and finally 6 countries, Botswana, Burundi, Ethiopia, Gambia, Namibia, and Niger, are listed as endemic but have not reported any cases in the past 20 years and have not yet received any support.

The 30 aforementioned countries received WHO support in the form of

  • Technical assistance. It is provided either by WHO staff or by WHO temporary advisers.
  • Access to diagnosis. This support includes the equipment, reagents, logistics, and funds to allow the national teams to reach HAT transmission areas to perform active case-finding surveys and set up passive surveillance. Since 2007, WHO has provided, free of charge, more than 35 percent of the CATTs used by national programmes.
  • Training. As part of capacity building, training was targeted at two technical levels: (1) training on site, hands on (410 technical staff from 23 disease-endemic countries were trained) and (2) participation in the International Course on African Trypanosomoses implemented in collaboration with the Association against Trypanosomiasis in Africa (105 programme managers or scientists from 22 countries have participated in either one of the five courses).
  • Access to treatment. This covers the provision of drugs as well as a patient's accessibility. During the past decade, WHO has covered the need of DECs by distributing, in collaboration with MSF-Logistics, 594,200 vials of melarsoprol, 576,375 vials of pentamidine, 477,542 vials of eflornithine, and 13,597 vials of suramin.

One main objective of WHO in the “access to treatment” initiative, supported by a new agreement between WHO and sanofi-aventis, was to reduce the use of the arsenic derivative melarsoprol for the treatment of second-stage gambiense cases by making eflornithine—actually the sole alternative to melarsoprol—accessible. Indeed, during the period 2003-2006, despite the availability of eflornithine and the toxicity of melarsoprol, it remained widely used, and 88 percent of the second-stage gambiense cases were treated with this drug (Figure A11-1). Only well-funded NGOs could afford the costly and complex use of eflornithine as first-line treatment, while NSSCPs used eflornithine exclusively to treat melarsoprol relapses. This was demonstrated during the period 2003-2006 by an eflornithine distribution ratio of 9 to 1 for NGOs versus NSSCPs (Figure A11-2).

A bar graph showing drug rate use for the treatment of second-stage T.b. gambiense: eflornithine versus melarsoprol (2003–2009)

FIGURE A11-1

Drug rate use for the treatment of second-stage T.b. gambiense: eflornithine versus melarsoprol (2003–2009).

A bar graph showing institutional rate use of eflornithine: National Sleeping Sickness Control Programmes versus nongovernmental organizations (2003–2009)

FIGURE A11-2

Institutional rate use of eflornithine: National Sleeping Sickness Control Programmes versus non-governmental organizations (2003–2009).

In 2006, a number of DECs requested the support of WHO to train their staff on the use of eflornithine and requested the provision of the necessary equipment to switch gradually from melarsoprol to eflornithine as a first-line treatment. Subsequently, a training of trainers was organized in southern Sudan, and a kit containing the drugs as well as all the materials needed to administer two full eflornithine treatments was designed by WHO and distributed with the collaboration of MSF-Logistics (WHO, 2009a). The kit for two eflornithine treatments weighed 40 kg at a cost of US$1,420. This particular effort in terms of logistics and funding allowed DECs to regularly decrease their use of melarsoprol for the treatment of second-stage gambiense cases. Consequently, in 2009 a 57 percent reduction in the use of melarsoprol was recorded (from 88 to 38 percent) (Figure A11-1), and the use of eflornithine by NSSCPs increased by 250 percent (from 20 to 70 percent) (Figure A11-2).

Nifurtimox, registered for Chagas disease, showed efficacy during compassionate use in melarsoprol refractory cases (Pepin et al., 1989; Van Nieuwenhove and Declerq, 1981). To simplify the eflornithine schedule, attempts were made to demonstrate that a therapy combining nifurtimox and eflornithine could contribute to a simpler administration of the drugs; some trials took place in DRC during the late 1990s (Bisser et al., 2007) and in Uganda during the early 2000s (Checchi et al., 2007; Priotto et al., 2006).

In 2003, an extensive nifurtimox/eflornithine combination treatment (NECT) clinical trial started in Congo and later in DRC involving MSF, Epicentre, the Special Programme for Research and Training in Tropical Diseases, and Drugs for Neglected Diseases Initiative (DNDi). The trial ended in 2008. Results indicated that NECT presented no inferior efficacy and safety compared to the eflornithine monotherapy (Priotto et al., 2009).

Following the inclusion of the NECT on the WHO Essential Medicines List in May 2009 (WHO, 2009b), NSSCPs requested WHO to train their staff to incorporate this new combination in their national policy. A training for trainers was organized in Kinshasa in November 2009 for French-speaking countries and another for English-speaking countries in Uganda in February 2010 (WHO, 2010a).

Thereafter, a new kit for NECT treatment was designed to continue to facilitate access to the best possible treatment. Thanks to the reduction of drug quantity and materials, using the same packaging form as for the eflornithine monotherapy treatment kits, a new kit for four full NECT treatments weighted 36 kg at a cost of US$1,440 was produced. This kit has already been distributed to nine countries (reporting together 96 percent of all T.b. gambiense cases in 2009): Cameroon, CAR, Chad, Côte d'Ivoire, DRC, Equatorial Guinea, Gabon, Sudan, and Uganda.

However, NECT does not change the paradigm of HAT treatment because it remains logistically complicated to implement. Nevertheless, it is anticipated that NECT will contribute to sustain the already observed decreasing trend of melarsoprol use for the treatment of second-stage T.b. gambiense infections (WHO, 2009c).

During the period 2006–2009, WHO promoted research for a better knowledge of HAT epidemiology and for the development of new tools. With that objective in mind, 23 agreements for “performance of work” were concluded with institutions of 11 countries (Belgium, Burkina Faso, DRC, France, Germany, Italy, Kenya, Malawi, Tanzania, Uganda, and the United Kingdom). In 2006, WHO and the Foundation for Innovative New Diagnostics19 signed a five-year Memorandum of Understanding to promote the development of simple and more sensitive and specific diagnostic tests. WHO took the responsibility to set up a specimen bank to facilitate the evaluation of relevant new diagnostic tools and to reduce the need for field trials. Currently, samples from 1,700 people including patients, seropositive suspects, and controls have been collected from 14 sites in Chad, DRC, Guinea, Malawi, Uganda, and the United Republic of Tanzania. More than 20,000 samples (including serum, plasma, white blood cells, urine, saliva, and cerebrospinal fluid) are stored in the central repository bank at the Institut Pasteur in Paris.

Strong collaboration has been established with groups working on the development of new drugs, mainly the Consortium for Parasitic Drug Development (CPDD)20 and DNDi21. In addition, the Division of Parasitic Diseases of the National Centre for Infectious Diseases, Centers for Disease Control and Prevention in Atlanta, Georgia; the Parasite Diagnostics Unit from the Institute of Tropical Medicine in Antwerp, Belgium; and the Research Unit of the Institut de Recherche pour le Développement based in the International Centre for Research and Development in Livestock in subhumid areas in Bobo-Diulaso, Burkina Faso, have been nominated as WHO Collaborating Centres.

In February 2008, WHO launched the initiative of the Atlas of HAT to map all reported cases for the period 2000–2009 at the village level. This initiative is jointly implemented with FAO in the framework of the PAAT. Presently, mapping includes 23 out of the 25 countries having reported at least one case in the last 10 years. In the two remaining countries, namely Angola and DRC, data processing is ongoing. The Atlas database also includes epidemiological information that can be used by NSSCPs, NGOs, and research institutions to monitor and evaluate the impact of control activities, to assess epidemiological trends, and to plan control or research activities (Simarro et al., 2010) (Figure A11-3).

A map showing classification of human African trypanosomiasis endemic countries according to cases reported in 2009

FIGURE A11-3

Classification of human African trypanosomiasis-endemic countries according to cases reported in 2009.

As a consequence of these activities, the number of new cases reported to WHO in 2009 dropped below 10,000 for the first time in 50 years (WHO, 2010b). This represents a decrease of 63 percent since 2000 (Figure A11-4). In 2009, only two countries reported more than 1,000 new cases, namely CAR and DRC, representing 11 and 73 percent, repsectively, of the total cases reported. One country, Chad, reported more than 500 but fewer than 1,000 new cases; 3 countries reported more than 100 but fewer than 500 new cases: Angola, Sudan, and Uganda; 11 countries reported fewer than 100 cases: Cameroon, Congo, Côte d'Ivoire, Equatorial Guinea, Gabon, Guinea, Kenya, Malawi, United Republic of Tanzania, Zambia, and Zimbabwe.

A bar graph showing evolution of reported cases of both forms of human African trypanosomiasis (1998–2009)

FIGURE A11-4

Evolution of reported cases of both forms of human African trypanosomiasis (1998–2009).

Finally, 19 countries listed as being HAT endemic reported no cases in 2009. Seven performed regular surveillance: Benin, Burkina Faso, Ghana, Mali, Nigeria, Sierra Leone, and Togo. Nine have no regular surveillance activities but reported no cases in decades, namely Burundi, Ethiopia, Gambia, Guinea Bissau, Liberia, Mozambique, Niger, Rwanda, and Senegal; however, these latter countries deserve an assessment to clarify their epidemiological situation. Two countries, namely Botswana and Namibia, are considered disease transmission free because of the recently implemented, successful tsetse elimination campaigns (Kgori and Modo, 2009; Kgori et al., 2006). Finally, Swaziland has been shown through an extensive tsetse survey to be free of HAT vectors (Saini and Simarro, 2008) (Figure A11-5).

An atlas of Human African Trypanosomiasis

FIGURE A11-5

Atlas of human African trypanosomiasis.

Discussion

During the past decade, the WHO public–private partnership (PPP) established in 2001 with Aventis Pharma and renewed in 2006 by sanofi-aventis made it possible to carry out extensive HAT control activities and to strengthen the capacities of NSSCPs. The PPP has been complemented by bilateral cooperation, by NGOs, and by support from Bayer AG. Furthermore, the interruption of civil wars and social upheavals has also substantially facilitated access to HAT endemic areas.

In 2009, the number of new cases of HAT reported to WHO has dropped below the symbolic number of 10,000, while in the period 2000–2009 the number of people screened increased because of the greater number of health care facilities involved in passive screening and through the improvement of the performance of active case-finding surveys. Owing to the improved knowledge of HAT distribution, WHO estimated in 2006 the factor gap between cases reported and cases infected to be three (WHO, 2006) instead of 10 as it was thought to be in 1995 (WHO, 1998).

Considering the next steps to be implemented, it is important to note that the disease situation is not homogeneous throughout the continent.

In several foci, the gambiense form of the disease has already reached a prevalence threshold compatible with the concept “eliminated as a public health problem.” To consolidate such a result and ensure sustainability, an adapted control and surveillance approach will have to be implemented within the national health system. Whereas, in other foci, HAT remains a public health issue mostly because of accessibility problems or security constraints (François Chappuis et al., 2010), and therefore reinforced control measures must be maintained using the classical vertical approaches with the participation of existing health care structures.

The rhodesiense form is a zoonotic disease involving cattle and game in the transmission cycle. Cattle movement is a continuous threat of disease transmission and spread and subsequently a source of outbreaks (Fèvre et al., 2001). Furthermore, wildlife in protected areas are niches for contamination; there is a continuous risk for park rangers, surrounding population, and visitors to become infected. Controlling this form of the disease requires a multisectoral approach. Therefore, it is crucial to reinforce local health care capacities for diagnosis and disease management as well as to establish effective coordination with veterinary and natural resources management services in charge of domestic, wild animals, and vector control.

Despite the encouraging results and exciting perspectives, the process remains fragile. At this stage, some obstacles are anticipated in the course of future control activities, and a few issues should be carefully considered:

  • The decline of contribution by NGOs and bilateral cooperation toward HAT control. During the period 2000–2009 there were 9 bilateral and 38 NGO HAT projects, while in 2010 there remained only 1 bilateral (DRC) and 5 NGO projects (CAR, DRC, Sudan, and Uganda). The positive aspect of this situation is the decrease of HAT-related emergencies and the substantial improvement of country self-managed HAT control activities.
  • The “tyranny of DALYS (Disability Adjusted Life Years)” expresses the lack of interest of donors when the burden of the disease is decreasing. Then supporting institutions withdraw not only from HAT control but also from HAT research. With the reduced amount of funds available for control, it seems obvious that the responsibility to give “the last strike to the dying beast” will exclusively rely on the overloaded and weak health services. Also, the loss of support for research will definitely eliminate any hope to get the needed, long-awaited new tools not only to accelerate the current control process but also to boost the involvement of health services in surveillance and control of HAT to sustain the achieved results. Such a situation will likely open the door for reemergence of the disease.
  • While the control of cattle as a HAT reservoir appears to be a reachable objective that would in turn allow the control of T.b. rhodesiense infections in affected areas (Kabasa, 2007), the control of the disease in wildlife and of the vector in protected areas and game reserves looks more complicated because of conservationist, ecological, and environmental considerations.
  • Because many patients remain to be treated, and they deserve to be treated using safe drugs, new safe and easy-to-administer drugs need to be developed also to facilitate control, to decrease the cost of distribution, to remove the risk of drug resistance, and to help ensure decentralized surveillance.

Furthermore, close monitoring is needed to assess the impact of climate changes and demographic evolution (Cecchi et al., 2009; Courtin et al., 2008) in HAT transmission.

Conclusion

By the end of last century, WHO and its partners developed a strong and successful advocacy program to secure access to diagnosis and treatment, ensuring the availability of funds and drugs to support DECs. As a result, during the first decade of the current century, great advances have been made in HAT control.

In 2007 a WHO informal consultation of the heads of NSSCPs held in Geneva reached the conclusion that “elimination of the disease as a public health problem” was possible (WHO, 2007). This conclusion was based on the achievements obtained, on the current understanding of the epidemiology of the disease, and on the willingness of African heads of states and government to eradicate tsetse and trypanosomiasis as stated when PATTEC was established in 2000.

The time has now come to sensitize stakeholders to the pertinence and ethical duty to embark on an “elimination process of HAT as a public health problem” despite difficulties, obstacles, and threats that are expected in this process. Without such a hammering approach, there is a risk of stagnation of control and surveillance as occurred in the late 1960s and led ultimately to the return of the disease.

Today WHO and partners are committed to reinforce and coordinate actions toward a sustainable elimination process (WHO, 2010c). Although there are still technical aspects to be solved, the “elimination of HAT as a public health problem” will require social peace, institutional support, and adequate funding for its implementation. These last conditions are not exclusive to the control, elimination, and sustained surveillance of HAT but also for the overall development of DECs, which would also contribute to the control of HAT.

When targeting the “elimination of HAT as a public health” problem, the goal should be recognized as a major achievement but must never be considered an endpoint. Without appropriate discrimination, the use of the word “elimination” may lead to risky conclusions. The disease believed to “no longer exist” will reach oblivion, placing in the background the required pressing efforts for a sustained and effective surveillance. It must be kept in mind that “elimination” is not synonymous with “eradication.” Elimination is only a point in time in the control process of the disease, at which stage the classical vertical control intervention approaches are no longer cost-effective. Thus, the national health system must take the ownership of sustaining elimination by integrating HAT surveillance in its services while keeping the capacity to react rapidly according to the analytical results of the surveillance outcome.

Elimination should be considered the beginning of a new process involving new actors. Therefore, elimination of HAT as a “public health problem” will require continuous efforts and innovative approaches. There is no doubt that new tools would facilitate the elimination process and the sustainability of results; thus, funding efforts for HAT control and research must continue based on a public health objective and no longer on the burden of the disease.

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This contribution is adapted from an article by the same authors to be published in PLoS (human African trypanosomiasis control and surveillance programme of the World Health Organization, 2000–2009: the way forward [Simarro, P. P., A. Diarra, J. A. Ruiz Postigo, J. R. Franco, and J. Jannin]).

Footnotes

16

This contribution is adapted from an article by the same authors to be published in PLoS (human African trypanosomiasis control and surveillance programme of the World Health Organization, 2000–2009: the way forward [Simarro, P. P., A. Diarra, J. A. Ruiz Postigo, J. R. Franco, and J. Jannin]).

17

See http://www​.fao.org/ag​/againfo/programmes/en/paat/disease​.html.

18

See http://www​.africa-union​.org/Structure_of_the_Commission​/depPattec.htm.

19

See http://www​.finddiagnostics.org/.

20

See http://www​.unc.edu/~jonessk/.

21

See http//www​.dndi.org/.

Copyright © 2011, National Academy of Sciences.
Bookshelf ID: NBK62512
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