Transmission

Onchocerciasis is caused by worms, Onchocerca volvulus. The adult worms measure nearly a meter long and live in coiled mating pairs in nodules under the skin. Reproducing adult females spawn about 2,000 immature worms every day. These tiny juvenile worms migrate throughout the skin and eyes, causing the various symptoms of the disease. Although they are damaging, these immature worms cannot mature to adulthood without being transmitted by a blackfly of the genus Simulium. This fly breeds in rapidly flowing streams and rivers, and thus the name "river blindness." The most important vector is Simulium damnosum sensus lato, which has a wide range throughout Africa and the Middle East. In East Africa, S. neavei also transmits onchocerciasis. There are many vectors in the Western hemisphere, but S. ochraceum, S. metallicum, S. oyapockense, S. guianense, and S. exiguum are among the most important. In the island of Bioko, the vector is S. yahense, Bioko form.

Blackflies serve as the intermediate host of the parasite. Flies ingest immature worms when they bite infected people. As the worms live in the fly, they mature sexually over the course of a week. Then, should the fly bite a person, the maturing worm will grow to adulthood inside the human body. Upon finding mating partners, the adults become encapsulated and produce more immature worms, completing the full transmission cycle.

The Disease Burden

The most severe consequences of onchocerciasis is blindness, which may affect one-third of the adult population of the most highly affected communities. The prevention of blindness was the main clinical reason for initiating the Onchocerciasis Control Programme (OCP) in West Africa in 1974 (Benton et al. 2002). Onchocerciasis causes several symptoms, including unrelenting itching, physical scars from constant scratching, de-pigmentation and thickening of the skin, impaired vision, and complete blindness.

Important pioneering studies in the last decade, sponsored by the United Nations Development Programme (UNDP), the World Bank, and the World Health Organization (WHO) Special Programme for Research and Training in Tropical Diseases (TDR), have shown that onchocercal skin disease (OSD) is associated with a greater degree of morbidity than was hitherto appreciated. These studies demonstrated that severe OSD causes suffering to millions of people, particularly to those in the forest zone, where the blinding form of the disease is less prevalent (Amazigo 1993; WHO 1995b). OSD not only causes psychosocial problems, ostracism, and stigma (Brieger et al. 1998b; Okello, Ovuga, and Ogwal Okeng 1995; Ovuga et al. 1995) but also has a demonstrably negative socioeconomic impact on the productivity of farmers, breastfeeding, and school attendance (Amazigo 1994; Benton 1998; Kim et al. 1997; Oladepo et al. 1997; Vlassoff et al. 2000).

The relative contributions of both ocular and dermal symptoms to the burden of onchocercal disease and their socioeconomic consequences are substantial (Kale 1998). The unbearable itching and blindness that accompany the disease hinder the ability of individuals to contribute to their own well-being, and they undermine the emotional and economic health of the household and the community. Consequently, onchocerciasis, which predominantly affects poor people in remote areas, can be directly linked to poverty.

The Socioeconomic Toll

In the 1970s, when investigations of onchocerciasis in the endemic villages and districts of West Africa began, scientists made astonishing and disturbing discoveries. More than 60 percent of the savanna population carried the parasite; 10 percent of the adult population and half of the males over 40 years of age were blind, 30 percent of the people were visually impaired, and early signs of onchocerciasis were common among children (WHO 1973, 1987, 1995a).

Scientists revealed the huge socioeconomic consequences of the high infection rates they had found.As village blindness reached epidemic proportions, it left too few able-bodied people to tend fields. Food shortages and economic collapse forced residents to abandon homelands in fertile river valleys. Moving to hardscrabble highlands and forested areas offered some protection from further infection, but then farmers struggled with poor soil and water shortages on overcrowded lands. Onchocerciasis often ultimately sent a prosperous community into poverty. Armed with this new knowledge about the economic impact, and with many fertile lands and water sources off-limits because of endemic onchocerciasis, development agencies made the disease a priority.

Rapid Epidemiological Mapping of Onchocerciasis

Continued research has led to the development of Rapid Epidemiological Mapping of Onchocerciasis (REMO), a tool that provides data on the distribution and prevalence of the disease. REMO is a simple, noninvasive, and practicable process that is easy to apply over a wide range of bioecological zones, with no sociocultural or religious restrictions. This tool was vital to rapid mapping and accelerating the scaling-up process of identifying endemic villages for mass treatment with ivermectin in control areas. Integration of REMO data into the Geographical Information System (GIS) allowed delineation of zones of different levels of endemicity, which is an important step in the planning process for onchocerciasis control. Zones, and communities in these zones, are included or excluded from the community-directed treatment with ivermectin (CDTI), depending on whether their levels of onchocercal endemicity reach the threshold set by the control program. Prevalence rates of infection in the OCP areas prior to control activities were high in all the countries.

Population at Risk and Population Infected

In 1995 it was estimated that 18 million persons were infected, of whom 270,000 were blind and about 500,000 persons severely visually impaired (WHO 1995a). However, the large-scale REMO that was undertaken by the African Programme for Onchocerciasis Control (APOC), covering the 19 remaining endemic countries in Africa, provides recent and more accurate estimates. From the REMO results it was estimated in 2004 that about 87 million persons were at high risk of contracting onchocerciasis in APOC countries. This figure is higher than the number at risk (about 58 million persons) reported two years earlier by Noma and colleagues (2002), when countrywide mapping of the disease had not been carried out in Angola and Burundi and had been implemented (only partially) in very few areas in the Democratic Republic of Congo and Sudan.

The results of REMO, also used to determine the number of infected persons in the APOC countries, showed that the mean infection rate was 38.2 percent, or approximately 37 million people. This represents almost three times the number estimated (13.7 million people) at the planning phase of the APOC program, when only partial data were available for few countries.

Onchocerciasis Control Programs

In 1970, funded by the UNDP, a team of WHO scientists and consultants began to lay the technical groundwork for a major regional initiative to defeat river blindness. By 1972 the international development community mobilized funds to aid in the control of the disease. In 1974 the affected countries and four agencies (the World Bank, the WHO, the Food and Agriculture Organization [FAO], and the UNDP) launched an unprecedented partnership. The "river blindness partnership" has had two distinct phases: the OCP between 1974 and 2002 and APOC between 1996 and 2010. The OCP had a dual mandate: to eliminate river blindness as a public heath problem and as an obstacle to socioeconomic development. The APOC mandate in East Africa and central Africa does not express the same socioeconomic development needs as did the OCP mandate in West Africa. This is because the strain of parasite prevalent outside the savanna belt is less likely to cause blindness. Instead, it exacts its toll in greater skin disease. The stigma and disability from these dermatologic effects are difficult to quantify, and humanitarian reasons alone were more than sufficient to justify the expense of control.

Vector Control

Onchocerciasis control is complicated by the long life of the adult worms, which remain fertile throughout most of their 10- to 15-year lifespan. The immature worms live in the skin for about two years, but their numbers are continually refreshed as long as adults are alive in the body. This means that even with instant and complete transmission control, the disease would not die out naturally for 15 years; hence, control attempts must last at least the life span of the adult worm. The control program in West Africa, the OCP, initially attacked the disease by killing the larvae of the flies that transmit the worms. It depended on killing these larvae over a long enough time that the adult worms would all die out. Then, when fly control stopped, biting flies would no longer ingest any parasites, and the transmission cycle would be broken. The key to this approach lies in reducing the fly population sufficiently to stop transmission and then sustaining the effort for two decades or more.

The principal strategy of the OCP from its inception was vector control. Covering Burkina Faso and six neighboring countries, the control began in 1974 in West Africa as a large regional project. Vector control, treating the breeding sites of disease-transmitting flies with larvicides, was the only available approach.

Prior control attempts dating back to the 1950s had shown that the disease is transmitted on a regional scale. The first projects were small, and the savanna was consistently reinfested. Accordingly, the OCP was established as a large program to cover entire endemic zones. Even this ambitious start was not sufficient; in 1986 the program doubled in size and was expanded to cover 11 countries in all.

Since blackflies migrate across international borders, the affected governments and international experts were convinced that only a regional program could control river blindness. Thus, the OCP targeted seven West African countries (Benin, Burkina Faso, Côte d'Ivoire, Ghana, Mali, Niger, and Togo; figure 15.1). With the collaboration and political commitment of these nations, control operations were planned. As the primary method of control, aircraft would spray environmentally safe larvicides around fast-flowing rivers—the breeding grounds of the intermediate host of the disease, the blackfly.

Figure 15.1

Prevalence of Onchocerciasis Infection in 1974 and Gradual Expansion, 1977–92 Source: Onchocerciasis Coordination Unit, World Bank.

Initially, operations covered 660,000 square kilometers in seven countries, an area believed to be large enough to contain the blackfly vector (WHO 1995a). However, in 1975, after three initial months of successful operations, many migrant blackflies from untreated watercourses reappeared, threatening to reintroduce the disease into the program area. Scientists found that the flies were coming from up to 600 kilometers away from the area being treated (Le Berre et al. 1990; WHO 1995a). In response, the program extended operations to another four West African countries (Guinea, Guinea-Bissau, Senegal, and Sierra Leone; figure 15.1). The program area increased geographic coverage from 780,000 square kilometers to 1.3 million square kilometers, enabling the campaign to increase the number of people protected from 10 million to 30 million.

Ivermectin Treatment and Approaches to Disease Control

The advent of ivermectin (Mectizan) and its donation by Merck & Co. in 1987, for as long as needed, provided a second string to OCP's control operations. The first extensive field studies on the suitability of the drug for use on a mass scale were conducted by the OCP (Awadzi et al. 1985). The favorable results of these studies led to the OCP's adopting mass distribution of Mectizan as an adjunct to vector control. In 1990 the program began full-scale distribution in extension areas—to the south and west of the original core area in West Africa—using mobile teams in jeeps plus local health staff support.

In this first step toward scaling up, OCP-paid local health professionals called communities to a central location for dosing. In more than 30 river basins, therapeutic coverage averaged about 65 percent in 1987, improving to more than 70 percent by 1995. However, it was expensive to use trained health staff at the local level. In light of high, recurring costs, the program considered various cost-recovery schemes to no avail. The answer to the high cost of mobile teams arrived indirectly. Invariably, when drugs were distributed, some villagers were away, either hunting, working, or traveling. In response, the program authorized the mobile teams to leave doses upon departure for absent community members, once it became clear that ivermectin's safety profile allowed unsupervised dosing. In the second step toward scaling up, national health services combined with local health staff to distribute the drug, forming a community-based distribution approach.

In some areas the OCP used ivermectin alone (Awadzi et al. 1985; Dadzie et al. 1990, 1991; Remme et al. 1989, 1990; Whitworth et al. 1991,1992) and effectively so. Ivermectin is effective against only the juvenile parasites, killing 95 percent with one dose. Even when a patient takes ivermectin, the adult worms continue to live, churning out offspring. However, because the juvenile parasites cause the disease, ivermectin relieves the symptoms and allows the body to begin healing itself. Treatment with ivermectin is required only once per year but must be taken for as long as any adults are still alive, up to 15 years. By killing almost all the immature worms, ivermectin also dramatically lowers the chance of parasite ingestion by biting flies.

The application of the two strategies by the OCP has led to the virtual elimination of onchocerciasis as a public health problem and as an obstacle to socioeconomic development in 10 of the 11 countries in which the program was carried out (figure 15.2), leading to the recognition of OCP as one of the most successful programs in the history of development assistance (Kim and Benton 1995). Figure 15.3 shows the other health interventions implemented using the CDTI network in APOC countries in 2004. By the end of the OCP, the program had covered 11 countries, protecting 40 million persons at risk and 1.3 million square kilometers of land. By the end of APOC in 2010, the program's two phases will have protected an estimated 150 million people in 30 countries.

Figure 15.2

Prevalence of Onchocerciasis Infection in 2002 Source: Onchocerciasis Coordination Unit, World Bank.

Figure 15.3

Scaling Up with Additional Interventions A community-directed network offers a key entry point for many health interventions in the most remote, rural communities. Phase II reaches the poorest of the poor in areas where National Health Services are weak (more...)

The initial efforts at mass distribution of ivermectin outside OCP were made by NGDOs. The first of the NGDO-facilitated ivermectin distribution programs in Africa was established in Nigeria in 1989 (Duke and Dadzie 1993). Many of the pioneering NGDOs were already well known through their activities in prevention of blindness and were already with the WHO Prevention of Blindness Programme.

The NGDOs soon recognized the need to coordinate their separate and independent efforts if they were to achieve their common goal. Therefore, in 1992 they came together to form the NGDO Coordination Group for Ivermectin Distribution. By 1995 the group needed considerably more resources than they could generate on their own for a significant expansion in the scope of their activities. Furthermore, the various NGDOs and programs used mobile teams and the clinic-based and community-based treatment with ivermectin in the distribution of the drug. These methods were proved inappropriate or not cost-effective for large-scale sustainable distribution of the drug for several years. In 1995 the Task Force on Onchocerciasis Operational Research of the UNDP, World Bank, and WHO Special Program for Research and Training in Tropical Diseases, in collaboration with the OCP, addressed the problem in a multicountry research study (WHO 1995b).

The study concluded that community-directed treatment with ivermectin (CDTI) was feasible and effective in a wide range of geographical and cultural settings in Africa, and likely to be replicable in other endemic communities in Africa. It recommended that this approach become a principal method for onchocerciasis control in Africa. (WHO 1996). The scaling up to community-directed treatment was a major turning point for the onchocerciasis control programs.

Two successful regional programs, APOC and the Onchocerciasis Elimination Program for the Americas (OEPA), were introduced to distribute ivermectin (Remme 1995; Richards et al. 2001). APOC was launched in 1995 to cover 19 countries in the remainder of infested Africa. In 1997 the program adopted the CDTI as its principal strategy for ivermectin distribution. In 2001, 42 million tablets of ivermectin donated by Merck & Co. were used in the 28 countries in Sub-Saharan Africa for onchocerciasis control. Ivermectin is distributed by community workers, trained and supported by the external partners.

In 1996 APOC had approved four CDTI projects, and by the end of 2003 the Programme totaled 107 projects to be implemented (table 15.1), of which 97 were CDTI projects. Sixty-two projects delivered more than 32 million treatments in 2003 alone (table 15.1). By 2010 the total treatments are expected to reach 90 million people. The distribution network is also being tested to deliver other health interventions. This enticing possibility opens the door to further scaling up to help control other diseases and presents the opportunity to deliver other basic health interventions in the river-blindness areas, all of which are remote, rural, and poor. Most are not reached by other programs, and some are not reached by the national governments themselves.

Table 15.1

Scaling up APOC, 1996–2003.

In 2003, through community-directed treatment, APOC countries achieved ivermectin therapeutic coverage of 68.1 percent on average in the targeted communities. It augmented these distribution efforts with a strong commitment to increasing capacity.

The introduction of ivermectin presented challenges and opportunities that became a catalyst for scaling up on all levels. It transformed onchocerciasis control from a technologically driven categorical health initiative to a community-directed process of treatment and empowerment of communities. This grassroots approach contributed, as shown in table 15.1, to high coverage of the population and empowered communities to take charge of their own health. It also planted the seeds for sustainability—absolutely vital for a disease that must be treated for at least 15 years to interrupt transmission. Systematic assessments of 48 CDTI projects in 10 countries (Cameroon, Chad, the Democratic Republic of Congo, Ethiopia, Malawi, Nigeria, the Republic of Congo, Sudan, Tanzania, and Uganda) at four levels—namely, the central level (the state, regional, and provincial levels of the different health systems in Sub-Saharan Africa), the district and local government authorities level, the subdistrict and frontline health facility level, and the community level—were undertaken between 2002 and 2004. These sustainability assessments were carried out with outside technical assistance. A total of 304 district and local government authorities and 468 communities were evaluated. The performance of health care service providers and community workers was assessed using quality-of-implementation indicators designed for the multicountry evaluation of CDTI. The results of these in-depth evaluations show that 35 (73 percent) of the 48 projects are making satisfactory progress toward sustainability, and 13 (27 percent) are not.

Conclusion

Over the last 30 years a large international partnership has successfully attacked onchocerciasis. This partnership has defeated the disease in 10 of the 11 countries in West Africa and is making progress in the remaining endemic countries in central Africa and East Africa. The program, spanning 30 countries across Sub-Saharan Africa, encompasses more than 107 projects to create a comprehensive approach to eliminating the disease as a public health problem. The onchocerciasis control programs have yielded the following results:

• 1989–90—60,000 people treated in 11 countries
• 1994—2 million people treated
• 2002 (end of phase 1)—40 million people protected in 11 countries; 600,000 cases of blindness prevented; 18 million children spared the risk of onchocerciasis
• 2003—33 million people treated in 69,641 communities in the APOC countries; more than 162,000 community distributors and 18,000 health workers trained or retrained
• 2010—a projected 102 million people and about 100,000 communities protected in 16 countries and a projected 150 million people protected in 30 countries.

Prior to 2002, when the OCP closed, 25 million hectares of relatively fertile land in the river valleys were freed for resettlement and for agriculture; the socioeconomic impact of OCP is considered to be enormous. More than 40 million people in the 11 countries were considered free from infection and eye lesions. Sixteen million children born after 1974, when OCP activities began, are free of onchocerciasis; more than 1.5 million people originally infected are no longer so; and more than 200,000 cases of blindness have been prevented.

The second phase of the studies to determine the impact of APOC are under way, but the program is considered to be highly cost-effective. The cost per disability-adjusted life year of APOC operations is US$6.50. A study is also being conducted to demonstrate the feasibility and cost-benefit of onchocerciasis elimination with ivermectin.

The community-directed distribution network can get primary health care to the poorest of the poor through simple, once- or twice-a-year interventions by nonmedical staff. In some areas, additional activities have been carefully tested and planned; in other areas, communities themselves took spontaneous action. Effective interventions exist, but they do not reach the people who need them most—the poor. Prior to the launching of APOC, not enough was known about what works to reach the poor, that is, what systems can ensure that poor and very remote populations have access to the benefits of health services, to available drugs, regardless of their locations.

Participating countries, donors, and the partnership's governing board have all endorsed the integration of community-directed treatment into existing health systems through other health interventions. Some countries, such as Uganda, have begun reorganizing their rural health services to use the community-based network as a national strategy. Some communities within the 30 African countries, along with NGDOs, such as Helen Keller International and The Carter Center, have begun distributing bednets to prevent malaria, and medications, including vitamin A, to prevent malnutrition, pediatric blindness, and death; Praziquantel to control schistosomiasis; and ivermectin and albendazole to control the transmission of lymphatic filariasis.

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