Onchocerciasis and Chagas' disease control: the evolution of control

Onchocerciasis and Chagas' disease control:the evolution of control via applied researchthrough changing development scenarios

D H Molyneux* and C Morelt

*Liverpool School of Tropical Medicine, Liverpool, UK and fFundacdo Oswaldo Cruz, Fiocruz,Rio de Janeiro, Brasil

This paper addresses the development of control strategies of two differentparasitic diseases and identifies commonalities which have contributed to thesuccess of regional intercountry programmes of onchocerciasis control in Africa,the Onchocerciasis Control Programme (OCP), and the new African Programmefor Onchocerciasis Control (APOC)1"3 and the Chagas' Disease ControlProgramme in the southern cone of South America4.

Correspondence toProf D H Molyneux,

Director, Liverpool Schoolof Tropical Medicine,

Pembroke Place,Liverpool L3 SQA, UK

The biological difference between Oncbocerca and Trypanosoma couldhardly be more extreme and although both infections result in chronicdiseases and are transmitted by vectors, there are few other similarities.Onchocerca volvulus is a filarial nematode transmitted by a short liveddipteran vector, Simulium, which breeds in fast flowing, well oxygenatedrivers, bites during the day depositing infective larvae in the skin, theintensity of the infection being related to the levels of transmission;pathology is, hence, dose dependent. The incubation period from time ofentry of an infective larvae to the maturity of an adult worm is 1-2 yearswhen microfilaria released by the adult worms, which are infective toSimulium, appear in the skin. Humans are the only host of O. volvulus. Incontrast, Trypanosoma cruzi is a protozoan kinetoplastid flagellatetransmitted by triatomine bugs. Triatomine bugs are Hemiptera of thefamily Reduviidae; the most important vectors deposit their eggs in cracksand crevices in mud walls, in ceilings or in furniture in houses. Nymphsemerge from the eggs and develop into adults through a series of instars(hemimetabalous life history). Each instar takes a blood meal and, hence,can transmit the infection at each feed after becoming infected. Theduration of the egg to adult through 5 instars can be from 6-12 months.Transmission is by the contamination of skin and mucous membranesfollowing the deposition of infective metacyclic trypanosomes on the skinof the host after the bite of the bug. The irritation provoked by the biteinduces scratching with infective metacyclic forms entering the bodythrough abraded skin around the site of the bite.

British Medical Bulletin 1998;54 (No. 2): 327-339 CThe British Council 1998

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Tropical medicine: achievements and prospects

A single infective faecal contamination can produce a T. cruzi infection,hence pathology is not dose dependent as in onchocerciasis. Differentstrains of O. volvulus and T. cruzi have been described. In O. volvulusstrains characterised by DNA techniques can cause different types ofdisease - blinding (savanna) or less bunding (forest) onchocerciasis5. Insome areas, onchocercal skin disease has been recognised as an importantpsychosocial and economic problem; onchocerciasis is a seriousimpediment to rural development, while its control has demonstrated thatresettlement of fertile valleys can improve agricultural productivity andenhance labour availability for the rural economy*.

T. cruzi strains displaying very different biological behaviour have alsobeen described7'8 and characterized biochemically and by moleculartechniques (zymodemes9-10, schizodemes11). These data allowed the analysisof the structure and behaviour of the different parasite populationscirculating in nature12"14 and to the proposition of potential correlationsbetween clinical-epidemiological data and strain characteristics15.

Control of transmission of both infections has enabled a generation ofchildren born since control began to be free of disease hence the trend totheir elimination as public health problems16. This implies a continuingcommitment to monitoring the impact of control by establishingappropriate systems to ensure the success of control is maintained andthat capacity exists to control any resurgence or recrudescence.

Characteristics of successful programmes

Onchocerciasis and Chagas' disease

The features which have been identified as of relevance to the success ofthe Onchocerciasis Control Programme (OCP) in West Africa have beendefined following an external evaluation in 19901. These characteristics(Table 1) are equally valid to the success of the Southern Cone Initiativein Chagas' Disease. Criteria are managerial, technical, and develop-mental18'23'37. They exemplify those factors which have contributed tosustained donor and government support when competition for resourceshas increased and absolute funds have been finite or reduced.

Both programmes are major exercises of organisation but representsimple concepts. The OCP has become more complex due to therecognition of blackfly migration, the development of insecticideresistance and the introduction of ivermectin. Chagas' disease control inthe Southern Cone relies on one strategy, the elimination of domesticand peridomestic foci of Triatoma infestans through house sprayingwith a pyrethroid19. The danger of insecticide resistance developing in

328 British Medial Bulletin 1998;54 (No. 2)

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Onchocerciasis and Chagas' disease control

Table 1 Characterise criteria of successful programmes

1 Long term perspective and time scale

2 Participating government/donor partnerships

3 Staff quality and commitment

4 Transparency of management and management systems

5 Government commitment

6 Targeted strategic and applied research with involvement of the scientific community

7 Government participation in drive to sustainability

8 Involvement of NGDOs/CSOs (Civil Service Organisations)

9 Financial phases allowing 5 year planning cycles

Triatomines are small and the risk of re-invasion limited as T infestansdoes not fly long distances. Both programmes rely on a wide geographicalcoverage to eliminate or reduce the risk of re-invasion.

Insect genetics/identification has played a role in both programmes asthe definition of the different biologies of closely related forms of vectorshas influenced strategy, e.g. (i) the relationship between insecticideresistance and cytospecies32; (ii) the comparative importance of forestversus savanna Simulium in transmission20; (iii) identification of 5.leonense in Sierra Leone as an effective but non migratory vector of anintermediately blinding form of onchocerciasis 21; and (iv) the distinctionbetween residual infestation of T. infestans from re-infestation on thebasis of genetic characteristics22.

The current objective of the Onchocerciasis Control Programme(OCP) in West Africa is: 'to control onchocerciasis as a disease of publichealth significance and as an obstacle to socio-economic developmentand to ensure that the participating countries are in a position tomaintain that achievement.'

The earlier objective was: 'to reduce the impact of onchocerciasis to asufficiently low level so that it no longer represents a public healthproblem or an obstacle to socio-economic development and also tomaintain and adjust control activities so as to stabilise the disease at atolerable level?

The evolution of the programme is described by Samba23, whilst Boatinet al37 show changes in policy and strategy diagrammatically.Commencing in 1974 after extensive preparatory studies between 1970and 1973 by the Preparatory Assistance to Governments (PAG) mission,the programme depended on vector control alone; one insecticide Abate(temephos), an organophosphate of low mammalian toxicity, was

British Medial Bulletin 1998;54 (No. 2) 329

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applied by helicopter to Simulium breeding sites every week in all riversystems of the programme area. Environmental monitoring to measurethe impact of Abate and latterly other insecticides on non-target faunawas introduced at selected sites from the beginning of the programme24.The continuous environmental assessment of the impact of insecticideson the aquatic fauna has been a feature of the programme satisfyingconcern that there is no long-term impact of pesticides on the aquaticenvironment. In addition, the development of an extensive and uniquedatabase on the insect, crustacean and fish fauna of the West Africanriver systems is available for future reference and as a guide to evaluatethe non OCP induced impact on river systems.

OCP was introduced as a 20 year programme as it was initiallyestimated that adult O. volvulus lived up to 20 years in the human host.Only continuous cessation of transmission would eliminate the humanreservoir of adult worms in the absence of a drug which killed adults -a macrofilaricide. This situation is not dissimilar from that in Chagas'disease where only vector control reduces transmission in the absence ofan effective drug to treat chronic disease - as in onchocerciasis, patientswith Chagas' disease remain reservoirs of infection to vectors if vectorsare not controlled. The advent of ivermectin, in the late 1980s as amicrofilaricide changed two approaches to the control of onchocerciasis.OCP's initial planning had anticipated a drug should optimistically (andrealistically) become available during the programme's life time; thearrival of ivermectin was a huge advantage as it had an impact on ocularmorbidity preventing blindness by reducing eye pathology, including theregression of anterior segment lesions as a result of regular treatment.The impact of ivermectin on transmission is, however, variable anddependent on intensity of disease in communities as measured by theCommunity Microfilarial Load (CMFL). Chagas' disease control wouldsimilarly benefit from such a drug if it was deliverable and effectivewithin a community scenario. The recent results with benznidazole seemin fact to point in such a direction26.

Since the inception of both programmes, and as a direct result of them,a significant increase in the knowledge of the disease, the parasites andthe vectors has been obtained. Evaluation of the impact of control hasbeen refined, the delineation of epidemiological situations established,the changes in vector distribution monitored and new insecticidesselected and evaluated in response to the appearance of temephosresistance and improved cost-effectiveness. The key developments inapplied and basic research, as well as the major decisions which havecontributed to the continuation and the refinement of controlapproaches are given in Tables 2 and 3.

Prior to the availability of Mectizan® (ivermectin) DEC (diethyl/carbamazine) and suramin were the only available drugs for onchocerciasis,

332 British Medical Bulletin 1998;S4 (No. 2)

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Table 3 Research and development on T. cruzi, triatomines and Chagas' disease

Important dates and steps in Chagas' disease control Impact Reference

1943 Creation of the legendary Bambuf field station of theOswaldo Cruz Foundation (then known as OswaldoCruz Institute) in the State of Minas Gerais, Brazil

The creation of the Bambul represents the Dias*first step towards the establishment of long- Silveira &term clinical and applied field research in Rezende*2

in Chagas' disease control

1948 First field trials of a 'new insecticide' (gamexane)establish the basis for the chemical control ofdomiciliated triatomine vectors

The results stimulate the 'Servicp Nacional Dias &de Malaria' to conduct the first 'prophylactic Pellegrino43

campaigns' against Chagas' disease in 1950

1950 Creation of the first National Control Programmesin Brazil and Argentina

Triatomine control starts in the States of Minas Silveira &Gerais and Sao Paulo, in Brazil, and the Provinces Rezende*2

of Chaco, La Rioja and Catamarca in Argentina

1953 Gentian Violet is proposed as a chemoprophylacticagent against transfusion-transmitted Chagas' disease

One of the first steps towards the control of Nussenzweigblood banks etar"

1974-1975 Creation of PIDE (Integrated Programme onEndemic Diseases) in Brazil, and TDR in Geneva;First meeting on Basic Research In Chagas' Disease,in Caxambu, MG, Brazil

trengthening of basic and applied R & Dactivities; straining of endemic country scientistsand development of critical mass of researchersworking in Chagas' disease control

Proceedings ofthe Caxambumeetings,Memohasdo InstttutoOswaldo Cruz,starting 1986

1975-1980 Conduction of national serologic and entomologic surveys in Brazil

1977 Chagas' disease control becomes a national

priority in Brazil

Production of the first reliable data on Camargo ef at"prevalence of human infection and vector Silveira Sdistribution Rezende*2

1982 Large scale field trials of alternative insecticides andformulations for the control of triatomine vectors

Substitution of chlorinated insecticides bysynthetic pyrethroids; better residual effectand acceptance, lower mammalian toxicityand better cost effectiveness

Silveira"

Oliveira-Filho"

1990 Multicentre double blind study for evaluation ofT. cruzi defined antigens as diagnostic reagents

Selection of better antigens which will form the Moncayo &basis of the commercial production of kits in Luquetti47

endemic countries for blood bank control

1991 At a landmark meeting in Brasilia, the Ministersof Health of the Southern Cone countries(Argentina, Bolivia, Brazil, Chile, Paraguay andUruguay) adopt a resolution calling for action toeradicate Tnatoma Infestans

US$ 90 million are allocated for vector control Kingman4*and US$ 6 million for blood bank screening. WHO/TDR4*The Initiative of the Southern Cone countries is WHO/TDR50

thus born, covering an area 6 times larger than thatcovered by the West African OCP. A total of US$ 206million is allocated from national sources of the sixcountries for control operations. It is estimated that thisinvestment will reduce the economic loss due toChagas' disease by US$ 4550 million

1991-1995 Industrial production of insecticide paints,fumigant canisters and triatomine sensor/detectorboxes in Brazil and Argentina

Increased efficiency of control programmesand cheaper surveillance phase

WHO/TDR"

1995 TDR meeting on the elimination of four diseases aspublic hearth problems (filariasis, onchocerciasis,leproxy and Chagas)

A long road from the creation of the Bambutfield station; over 50 years along the path'Investigate, eliminate, eradicate'.

WHO/TDR50

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and were inappropriate for use in communities. Similarly Chagas' diseasedrugs are toxic and treatment of chronic T. cruzi infection remainsunavailable, hence the human reservoir of the parasite remains - asituation similar to that of onchocerciasis where an effective macro-filaricide is not available. The search for appropriate drugs for Chagas'disease continues51r52. Whilst Nifurtimox and benznidazole can be used fortreatment of acute Chagas' disease their cost, availability, toxicity andduration of hospitalisation precludes their use as significant public healthinterventions53. In addition, the problem of blood transfusion and organtransplantation transmission in Chagas' disease, has brought the disease tothe forefront of recognition not only as a rural/peri-urban disease but onewhich impinges on hospital culture and practice. Medical leverage hasemphasised the importance of screening at blood banks and blood bankcontrol. Transplant medicine requires an awareness of donor background,blood donor policy, and the implications of immune suppression ontransplant recipients. These particular problems specific to Chagas' diseasehave enabled investment in screening to parallel the necessity for thescreening of other blood-borne diseases (such as HTV, hepatitis, malaria) inblood banks with the consequent standardisation of serological tests, useof gentian violet in donor blood and screening of transplant donors44-49,although it is recognised that the great majority of transmission (80%) isvia the vector42*53.

T. cruzi infections and Chagas' disease have demonstrated a remarkablebiochemical, molecular and clinical heterogeneity55"57. This heterogeneityof biological and clinical features is not dissimilar to that of onchocerciasisin Africa39. However, the zoonotic nature of T. cruzi means that eradicationsensu strictu is never achievable. The control programme, therefore, targetsareas where Chagas' disease is of significant public health importance, andwhere eradication of Triatoma infestans might be achievable. Historicaloutlines have described how the national Brazilian campaign developedsince the creation of the Batnbui field station in the State of Minas Geraisin 1943 - where the basis for the chemical control of vectors wasdeveloped - to the times when resources for vector control were allocatedat national level notwithstanding earlier programmes at state level ofvarying efficiency4'17>42. Such early programmes in west Africa were alsocritical to provide experience for later intercountry planning for OCR

The strategy for Chagas' disease control is the spraying of houses withresidual insecticides to eradicate the strictly domestic species T. infestansand to reduce domestic infestation rates so that transmission of T. cruzito man does not occur in areas where vector species retain sylvaticecotopes, e.g. Panstrongylus megistus, T. brasiliensis, T. sordida and T.pseudomaculata5S.

Early vector control activities used BHC (Lindane) an organochlorine,applied at 500 mg/a.i./m2. Organophosphates, such as fenitrothion, and

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carbamates could also be used but as no insecticide resistance has beendetected in bug populations alternative insecticides (in contrast toonchocerciasis control) were only considered when synthetic pyrethroids(deltamethrin, cypermethrin, lambdacyhalothrin, cyfluthrin) becameavailable and were shown to have a better residual effect, betteracceptance, potential lower mammalian toxicity and more cost effective-ness4*. A similar approach to cost effective insecticide application has beendeveloped by OCP33 using a rotational insecticide strategy to avoidblackfly resistance development, thereby increasing susceptibility totemephos, the most cost effective and environmentally acceptablelarvicide. The vector control strategy in Chagas' disease has beenreviewed59 in the context of the impact of synthetic pyrethroids onTriatominae where a key difference is that pyrethroids are more effectiveat lower temperatures (compared with other insecticides), hence efficacywill be retained longer if spraying takes place during the colder months.The view that highly residual formulations are required has resulted inconsiderable research to produce slow release materials46. Guillen et al59

point out that while organochlorines had great stability and moreprolonged residual effects, pyrethroids seem most effective at eliminatingTriatominae because of more effective initial impact. This suggests thatthe most effective strategy would be to achieve as wide a degree ofcoverage as possible to eliminate possible re-invasion sources rather thanrequire repeated applications to eliminate re-infestations.

The Chagas' Control Programme's different phases of activity arerecognised as similar to those of the former malaria control programmes;the preparatory phase, the attack phase and vigilance phase59. Preparatoryphases in Chagas' control require extensive mapping and logistic planningand parallels the Preparatory Assistance Mission to Governments (PAG)in OCP between 1970-1973 and current mapping of hyper andmesoendemic communities in APOC countries3. The attack phase in thefirst year requires spraying of all homes, whether infested or not, which insubsequent years is followed by evaluation of the presence of the domesticbug populations with a respray if infestations are detected - the'evaluation attack phase' control infestation rates are below 5% and no T.infestans are found4. The annual cost of the attack phase in Brazil wasestimated at US$ 25 million which involved the spraying of 600 000homes annually. The vigilance phase indicates in Brazil that 85% of over700 municipalities have eliminated T. infestans infestations17. Figures inthe other southern cone countries indicate similar levels of control inChile, Argentina, Uruguay and Paraguay whilst serological evidence alsoindicates reduced incidence and prevalence as measured in cohorts of thepopulation born since control began whilst acute cases are declining61.Domestic populations of other species such as P. megistus and T. sordidahave also declined62.

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As with OCR, Chagas' control has been a highly organised, plannedand well resourced activity; both programmes recognise the need toencourage a decentralised approach and a participative communitybased reporting system for detection of bug recrudescence and re-invasion. Common problems are: (i) the difficulties of detecting low bugpopulations and in the OCP area continued transmission or earlyrecrudescence of transmission37 with the consequent expense ofmonitoring and surveillance; (ii) as control continues and diseases arereduced as a public health problem, they are no longer a priority; (iii)the influence of human migration or re-invasion and the interpretationof epidemiology; (iv) re-invasion of bugs or infected black flies fromoutside areas under control25'59; (v) the persistence of undetected vectorpopulations37; and (vi) changes in environment through replacement ofnatural ecosystems by ranching, agricultural projects, hydro-powerdevelopment, deforestation or reforestation in Chagas' disease. In WestAfrica, vector population distribution has been influenced by extensivedeforestation with consequent impact on distribution of savanna blackfly populations with the potential for southerly spread of compatiblesavanna bunding strains of O. volvulus. Hence, in both diseases, theimpact of control must be compared with continent-wide demographic,social and economic trends, as well as changing health systems and therecognition of the need for a 'devolution' or transfer process to ensuresustainability at the lower levels of the health systems with appropriatecommunity education and involvement.

In parallel with insecticide spraying, which is the basis of both theprogrammes, the interest and commitment of WHO/TDR to research onChagas' disease resulted in additional tools to supplement spraying. Thedevelopment of fumigant canisters (produced in Argentina) andinsecticidal paints provided additional approaches to vector control moreeasily deployed by communities whilst simple and cheap monitoringdevices have been deployed for bug detection46.

Both Chagas' disease and more recently the OCP, but particularly thenew African Programme for Onchocerciasis Control (APOC), haveinvolved the non-governmental organisations in their control strategies.APOC for the distribution of Mectizan® in recognising that NGOactivities are an increasingly important dimension in health provision. Inboth OCP, APOC and the Chagas' Disease Control Programme thevalue of interventions through cost effectiveness analysis hasdemonstrated the value of a long-term vertical programme in terms ofeconomic rates of return6,17.

In research towards more cost effective and devolved control, Chagas'disease has benefited from applied research on the efficacy of newpyrethroid insecticides, of new models of delivery of insecticides lessdependant on historically costly vector control structures and on the

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development of standard serological tests so comparable evaluation ofselected target groups can be undertaken throughout the control areathereby unifying reporting and assisting interpretation of success.Research has demonstrated that continued surveillance is critical andthat vectors other than T. infestans can present a persistent problem.Preparatory research activities for control of Chagas' disease in Andeancountries and in Central America is under way18, whilst APOC is seekingto develop country plans and time limited 5-year Community DirectedTreatment projects with Mectizan® to ensure sustained distribution bycommunities to reduce the disease to one of limited public healthsignificance in terms of both ocular and skin disease3. The approachesto successive programmes for Chagas' disease recognise the difficultiesof more complex insect biology and the zoonotic nature of the causativeorganisim but also the feasibility of local eradication of Rhodniusprolixus in some situations a parallel approach to isolated blackflypopulations of S. neavei in Uganda and possibly some Tanzania popul-ations of S. damnosum.

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Onchocerciasis and Chagas' disease control: the evolution of control

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