Sleeping sickness and its relationship with development and biodiversity conservation in the Luangwa Valley, Zambia

Historical development in the Luangwa Valley

Identification of Trypanosoma brucei rhodesiense and initiation of the sleeping sickness commission

The first documented case of Rhodesian sleeping sickness, as caused by Trypanosoma brucei rhodesiense, was published in 1910 [8]. A mineral prospector, W. Armstrong, became infected with sleeping sickness after visiting the Luangwa Valley in 1909. Laboratory investigations led to the discovery of a new form of human-infective trypanosome with differing virulence to T. b. gambiense, the only known cause of HAT at the time. Discovery of this new parasite, along with many other cases of trypanosomiasis in people visiting the Luangwa Valley, led to establishment of a sleeping sickness commission by the BSAC in 1911 [9]. The objective was to identify the vector and investigations were based at the abandoned government post at Nawalya (now Nabwalya, situated in Munyamadzi GMA) and on the western plateau at Ngoa.

The commission identified G. morsitans as the vector and showed a considerable percentage of wild animals were infected [9]. This was the first demonstration of trypanosomes in wild animals under natural conditions and antelope were considered to be the principal reservoir of the human trypanosome. Domestic livestock were scarce or non-existent in the Luangwa Valley at this time and cattle were recorded in only one village by the commission.

Subsequent patterns of infection in the Luangwa Valley

Sleeping sickness in the Luangwa Valley has been characterised by low levels of endemic disease with occasional outbreaks and epidemics [21,22]. Epidemics of sleeping sickness resulted in a large area being declared a ‘Sleeping Sickness Area’ and closed to hunting by non-residents from 1912-1925 and from 1927-1934 [11]. Around this time Lane Poole stated that “the presence of tsetse fly in great density and the occurrence of sleeping sickness in some localities deferred the traveller” [19]. He described a severe epidemic of sleeping sickness affecting the people of Kakumbi in 1918 and numerous village relocations due to the presence of disease.

HAT has been most common in the north of the Valley in the Isoka and Chama Districts [21]. Buyst concluded that several factors could explain increased likelihood of disease in the north including; collision of an expanding fly belt with the human population, climatic stresses in the north of the valley and lack of abundant game animals as tsetse food source, and migratory wildlife movements. In an outbreak in Kasyasya village in Isoka District in 1982, some 11 cases were reported from a total population of 75 people [23]. Point prevalence of HAT in the northern Luangwa was estimated at 0.58% (using several parasitological methods and an indirect fluorescent antibody test (IFAT)) [22]. Disease incidence was estimated at 1%, with a 40% cumulative lifetime (40 years) risk of infection.

HAT has also been reported in Petauke District, lower Luangwa Valley, and an early sleeping sickness focus was recorded at Hargreaves (Figure 2). Hargreaves was a Luangwa River crossing point which was abandoned due to its reputation as a source of sleeping sickness [24]. In 1971 an outbreak occurred resulting in 16 deaths out of 36 reported cases and reports emerged of ‘morbid mystique’ surrounding HAT [24], due to an extreme reluctance of people suffering from sleeping sickness to seek medical treatment. There was a belief that treatment would not result in a cure [25] and the occurrence of sleeping sickness in the Luangwa Valley has been associated with witchcraft and related accusation [26]. Examination of Trypanozoon taken from wild hosts between 1980 and 1983 using the blood incubation infectivity test (BIIT) [27] showed a large number of potentially human-infective parasites from animals in the upper Luangwa Valley around Kampumbu and Chibale (121) and fewer in the mid-Luangwa Valley around Mpika, Luchembe and Nabwalia (44). Very few potential human infective parasites were identified in Kakumbi, mid-Luangwa Valley and it was concluded that the risk in this area was small.

A controversial characteristic of sleeping sickness in the Luangwa Valley is the sub-acute nature of infection and existence of asymptomatic human carriers, postulated to be the result of long-term exposure and co-evolution [21,28,29]. A case-control study for sleeping sickness risk-factors in the northern Luangwa Valley found no increased risk in people born outside the valley and other studies have also questioned the existence of this sub-acute form of the disease [30-32].

More recently, official figures for sleeping sickness under-estimate the true disease incidence. Misdiagnosis and lack of diagnosis are common, in part due to the high incidence of retroviral disease [33].The distribution of HAT cases from 2000 to 2009 has been mapped as part of the HAT Atlas initiative, including the Luangwa Valley [34]. Within Zambia a total of 82 cases were recorded (including cases exported outside Zambia) with between 4 and 15 cases per year [34]. Cases have been reported in foreign tourists visiting the Luangwa Valley which could potentially impact negatively on tourism related activities [35]. A recent study estimated that approximately 416,000 people are at risk of contracting T. b. rhodesiense infection in Zambia although the risk is considered to be low in many areas [36].

The wildlife reservoir for trypanosomiasis

More recently, an extensive survey into the trypanosomiasis reservoirs in wildlife throughout the Luangwa Valley was undertaken, using novel molecular techniques for parasite identification [12]. Human-infective T. b. rhodesiense were confirmed in buffalo (Syncerus caffer) for the first time and were also identified in bushbuck. Bushbuck are considered the most significant reservoir host for T. brucei s.l. showing high levels of infection, along with waterbuck and the carnivores. Bovidae, and in particular greater kudu, were found to comprise the most important members of the host community for T. congolense. The prevalence of T. vivax was lower with waterbuck the most significant host identified. Other investigations in the Luangwa Valley have identified human serum resistant T. b. rhodesiense in warthog [38], zebra and impala [39]. T. brucei has been identified in four out of 75 hippo [40] and one lion [41]. The ecological factors associated with the epidemiology of wildlife trypanosomiasis have been reviewed in detail [42].

Trypanosomiasis control and vector investigation

Regional control measures

Despite successes in controlling tsetse in many areas, the absence of effective barriers to re-invasion and the protracted war in the region between Zambia, Mozambique and Zimbabwe meant that many gains from earlier control measures were lost. As a result, several international collaborative efforts to eradicate tsetse were attempted. The first launched by the Food and Agriculture Organisation (FAO) in 1972, aimed to eradicate tsetse from Africa within ten years using insecticidal spraying [49].

Following the failure of this Africa wide programme to achieve its very ambitious aims, a regional approach to tsetse control in southern Africa was proposed. This proposal, referred to as the Regional Tsetse and Trypanosomiasis Control Programme (RTTCP), was funded by the European Union from 1984 and ran until the late 1990s. At inception, the objective of RTTCP was the eradication of tsetse from the entire common fly belt of southern Africa with a view to encouraging cropland farming, tourism and livestock production [50]. The regional approach was extractive and never incorporated indigenous means of either understanding or controlling tsetse. The focus changed to tsetse control in prioritised areas when it became clear that regional eradication was not achievable. By the end of the RTTCP it was widely considered ‘that the farmer must go it alone’ with respect to management of tsetse control.

South Luangwa national park (SLNP) was selected as a site for monitoring the effects of the RTTCP and as a consequence research into tsetse and trypanosomiasis was undertaken in the park and surrounding GMA. Considerable data was generated that included investigations into the distribution of trypanosome infections [51], age prevalence of cattle and tsetse populations [52,53], the dynamics of trypanosome infections [54] and the distribution of tsetse species using remotely sensed data and climate data [55,56]. Tsetse densities recorded during monitoring in the SLNP were high, illustrating the suitability of habitat in the Luangwa Valley. The graphs in Figure 3 and Figure 4 below illustrate monthly mean tsetse counts recorded in 1996 and 1997 for G. pallidipes and G. m. morsitans sampled using Epsilon traps. Clear seasonal fluctuations in counts are demonstrated in the two vegetation types sampled, particularly for G. m. morsitans. Glossina brevipalpis were also recorded during this period, but only in very small numbers because of the sampling method used and the occupation of a niche habitat close to rivers.

A new international collaborative approach to tsetse control was launched with the formation of the Programme Against African Trypanosomiasis (PAAT) in 1997. This programme sought to adopt a common strategy that would lead to a harmonised and standardised approach to trypanosomiasis control [49]. Demonstrating African governments continued support for tsetse eradication, the Organisation of African Unity (OAU) agreed to act collectively in a Pan-African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC) “in order to render Africa tsetse-free within the shortest possible time” [49].

Early land use strategies by local communities

High tsetse and trypanosomiasis challenge in the Luangwa Valley meant that agricultural practices involving livestock were not possible and the early settlers, the Bisa, successfully developed alternative strategies to manage the environment around them and to survive in a somewhat hostile environment [10]. These strategies to manage and utilise the local wildlife evolved and hunting became a main element of their culture. These strategies served to supplement dietary requirements (especially in times of drought), and to limit crop damage from wildlife. The advent of the trade in ivory, meat and hides by early explorers and traders lead to a change in the degree of utilisation of the wildlife, as well as the methods used. There were no restrictions on the numbers of wildlife killed by these early traders and the minimal annual commercial off-take of elephant from the Luangwa Valley in the mid-19^th century has been estimated to have been approximately 2200 animals [57].

Creation of protected areas

The onset of the colonial era, however, brought the imposition of laws and regulations to control the utilisation of wildlife and sought ‘to protect the environment from the perceived threat from the local people’. These laws were implemented on a ‘fines and fences’ approach that can be traced back to the creation of the world’s first national park, Yellowstone, in 1872 [58]. Many of the inhabitants of the valley became marginalised and alienated by these new laws and many still have a negative view of conservation today [10].

The first set of regulations were adopted in 1900 [11] and the first game reserve was created in the Luangwa Valley in 1904 to protect giraffe populations. No development took place and it reverted back to its unprotected state in 1913. It was not until 1942 when control of the wildlife estate was passed over to The Department of Game and Tsetse Control that game reserves were once again created in the Valley. The southern and northern sections of the Luangwa Valley Game Reserve were gazetted and Controlled Hunting Areas were created. These measures were successful in conserving populations albeit through a top-down enforcement approach. After independence, the status of the game reserves was changed to that of national parks in 1972 and a system of GMAs replaced the Controlled Hunting Areas. In 2000, the semi-autonomous Zambian Wildlife Authority (ZAWA) was created to replace the National Parks and Wildlife Service.

The current status of protected areas

Four national parks are recognised in the Luangwa Valley (Figure 1). The function of the national parks is to provide a breeding environment from which the wildlife population may ‘spill over’ into to the GMAs for consumptive purposes [59]. Non-consumptive tourism is very popular, especially in South Luangwa which is the highest revenue-earning park in Zambia (17853 international and 6076 domestic visitors in 2004 [60]). The Luangwa Valley also contains nine GMAs, many of which are classified as prime hunting areas. Together they cover a much larger area than the national parks and contain a wide diversity of wild flora and fauna. Consumptive utilisation of wildlife is allowed, but is regulated by the ZAWA. There are no restrictions on human settlement or agricultural practices in the GMAs. Theoretically, this policy could increase the number of people at risk of contracting sleeping sickness due to their proximity to intact tsetse habitat, but it must be remembered that people have lived in these areas for centuries and the creation of GMAs did not significantly alter populations. In conservation terms, GMAs have a conflicting function in that they are intended to provide buffers and wildlife corridors around and between national parks, but at the same time permit the utilisation of the wildlife contained within them for economic purposes.

Community based natural resource management

The Luangwa Valley is notable for the degree of community engagement in natural resource management and provides some of the earliest examples of Community Based Natural Resource Management (CBNRM) programmes in Africa. From as early as 1941, local valley inhabitants received some benefit from wildlife under the colonial authority. In 1949, a ‘conducted hunting party scheme’ was initiated by Norman Carr with revenues going to the Native Authority [61] and the native authority reserve was created in Nsefu [11]. Despite these early progressive and inclusive policies, centralised control became strengthened towards the end of the colonial administration and during early independence. As a consequence of the poaching crisis of the late 1970s and early 1980s, two new approaches to CBNRM were trialled. The Luangwa Integrated Resource Development Project (LIRDP) and the Administrative Management Design for Game Management Areas (ADMADE) heralded a new era for community participation [62]. Although these programmes achieved mixed success [63], the CBNRM concept was strengthened under the Wildlife Act 1998 through the creation of Community Resource Boards and Village Action Groups managed by the newly created ZAWA. Such schemes are important in terms of sleeping sickness control, particularly after government policies of decentralisation and privatisation of veterinary services have left local communities to initiate control measures.

Another major development in the Luangwa Valley has been the move towards the creation of the Malawi/Zambia Transfrontier Conservation Area (TFCA) with the support of the International Union for Conservation of Nature (IUCN) [60]. If successful it is likely to improve biodiversity conservation and provide additional income for local communities through eco-tourism. It should also facilitate cross-border cooperation on disease control measures enabling more effective strategies for management of trypanosomiasis.

Agricultural development

Agriculture, at subsistence or semi-commercial level, is the main occupation, revenue provider and source of food for the local valley inhabitants [64]. The Luangwa Valley is a challenging environment for agriculture with recurring droughts and widespread food insecurity [10]. Livestock keeping remains rare in the Luangwa Valley, due to the high trypanosomiasis challenge, problems with predation, a generally poor environment for domestic livestock, lack of veterinary support services and the prevalence of other diseases. A range of subsistence crops are grown including: maize, rice, beans, soya, groundnuts, sorghum, millet and cassava. Honey is harvested from wild bees and bee keeping is an increasingly popular livelihood strategy. Charcoal production is common in some parts of the valley, particularly Nyimba, Petauke and Chinsali districts which are situated towards centres of higher human density [42]. Many areas of the Luangwa Valley are highly suited for growing cotton [11] which is a popular cash crop for many communities. Restricted access to outside markets severely limits the benefits attainable in the Valley from agriculture.

A new interface in the Mid-Luangwa Valley

Although small in relation to the Luangwa Valley itself, this new interface represents a significant diversion from traditional land use practices and has brought into question the widely held belief that livestock keeping is not possible. It is the first time large numbers of domestic livestock have been successfully kept since the rinderpest outbreak in the late 19^th century. It is an important development in terms of trypanosomiasis control as epidemics of AAT are more likely at new human/wildlife/livestock interfaces such as this [14].