patterns of epidemiology and control of onchocerciasis in...
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Journal of Helminthology (1997) 71 91-101 91
Patterns of epidemiology and control ofonchocerciasis in West Africa
B Boatin1 DH Molyneux2 JM Hougard1 OW Christensen3ES Alley1 L Yameogo1 A Seketeli1 and KY Dadzie1
World Health Organization Onchocerciasis Control Programme BP 549Ouagadougou Burkina Faso 2Liverpool School of Tropical Medicine
Pembroke Place Liverpool L3 5QA UK 3World Health OrganizationOCP Liaison Office 1211 Geneva 27 Switzerland
Abstract
This paper summarizes the work of the Onchocerciasis Control Programme(OCP) in West Africa a programme which over a 22 year history has reduced thepublic health problems of blinding onchocerciasis in eleven countries of West Africathrough vector control and more recently ivermectin distribution The paperemphasizes the different approaches to control the programme has developed inthe different parts of the programme area which have been determined by theepidemiology of the disease (savannaforest form) the migratory characteristicsof the vectors intensity of the disease before commencement of treatment thecombined impact of vector control and ivermectin and the likelihood of infiltrationof infective blackflies from outside the programme area The programme hasconstantly monitored the impact of operations on the trends in prevalenceincidence annual transmission potential ocular morbidity and species of flypopulations and as a result has identified areas where special interventions arerequired until the programme comes to an end in 2002 The paper illustrates thechanges in intensity of infection as measured by community microfilarial loadand annual transmission potential over the duration of the programme controlactivities The paper also defines and justifies the control strategies in differentareas and identifies areas for special interventions
Introduction
Onchocerciasis (river blindness) is a disease caused bya filarial nematode parasite Onchocerca volvulus transmittedby blackflies (Simulium species) There are approximately175 million people infected and of these it is estimated thereare some 270000 blind (in 26 countries in Africa Yemenand six in the Americas) (WHO 1995) Different patternsof epidemiology exist and the stratification of the disease isshown in table 1 Such patterns are associated with differentstrains of the parasite (forest v savanna) (Duke et ah 1966Zimmerman et ah 1992) and different vectors (cytospeciesor species) (Crosskey 1987 WHO 1995) the abundance ofthe vectors and degree of anthropophily their vectorial andmigratory capacity (Le Berre et ah 1990 WHO 1995)
Author for correspondence
The parasite lives as adults (males and females) insubcutaneous nodules The females when fertilizedproduce millions of microfilaria (embryos) about 250-300um in length which live predominantly in the skin butmigrate throughout the intercellular fluid and reach theeye leading to the characteristic ocular symptoms whichlead to blindness In addition the presence of microfilariaein the skin causes intense itching thickening anddepigmentation of the skin and loss of elasticity whilstother clinical manifestations such as hanging groin andelephantiasis of the genitals also occur (see WHO 1995)
Approaches to control
The Onchocerciasis Control Programme (OCP)conceived in 1969 and launched in 1974 had as its objectiveto eliminate onchocerciasis as a disease of public health
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92 B Boatin et al
Table 1 Stratification of global onchocerciasis epidemiology and control
Geographical locality
AfricaSouth of SaharaOnchocerciasis ControlProgramme (OCP)countries
1 Original areas - BeninBurkina Faso Cotedlvoire Ghana MaliNiger Togo2 Extension areasSouthern areas of GhanaTogo Benin westernextension Guinea GuineaBissau Sierra LeoneSenegal
Non-OCP countries3 Nigeria to Sudan4 West and EquatorialAfrica Guinea-Bissau toGabon Rain forest5 Zaire Basin6 East Africa highlandsEthiopia to SouthernMalawi
Central AmericaGuatemala Mexico inwell defined foci Crossborder movement ofmigrant workers mayspread the disease
South America1 Brazil S Venezuela2 N Venezuela3 Ecuador Colombia
YemenDistributed along wadis
Epidemiological
Savannah woodland ofnorthern tropics Hyper-endemic villages close torivers Historicallyassociated with highblindness rate resultingin depopulation
Major vectors in savannaS damnosum and Ssirbanum Annualtransmission potential ormore than 100 associatedwith blindness riskHighly migratory
In forest areas lessblinding form of Ovolvulus transmitted byforest vectors S soubrenseS yahense S sanctipauli Ssquamosum S leonense(Sierra Leone) which areless efficient and non orless migratory
Anthropophilic Sochraceum in highlandfoci S metallicum morezoophilicalso involvedInefficiencyas vectordue to buccal armaturecomplicated byabundance
1 Primary vectors Soyapockense and Sguianense2 Primary vector Smetallicum3 Primary vector Sexiguum12 Secondary vector Sexiguum
A member of the Sdamnosum complex
Operational
1 Vector control byweekly aerial larvicidingfor 14 years eliminatesadult worms in humanreservoir Ivermectin forrecrudescence orundetected foci2 Combined vectorcontrol and ivermectin for12 years projected toreduce disease to non-significant levelIvermectin alone in areasof low CMFL (lt10) whereno invasion ofSimulium threatensoriginal OCP area345 Ivermectin throughcommunity baseddistribution systems6 or 3-5 Focal vectorcontrol could achieveeradication of S damnosumor S neavei
Control by ivermectindistribution via nationalprogrammes throughtwice yearly distribution
Vector control not feasibleIntegration of ivermectinwith other programmes
Control initiated
Disease management
1 Vector control applieddue to lack of availabilityof drug for large scaleuse till 1986 Thereafterivermectin to reduceinfection and preventdevelopment of ocularlesions2 Ivermectin throughoutfor extended periods upto 20 years as ivermectindoes not interrupttransmission3 Impact of ivermectin onskin disease and othermanifestations of Ovolvulus infection to beassessed
Ivermectin based
Ivermectin based
Ivermectin based
Prevention
1 Maintain surveillancesystem for recrudescenceusing tests for earlydetection of transmissionInstitute ivermectin ifappropriate Establishappropriate surveillancevia integration inpublic health systemsPossible detection of earlytransmission by detectionof infective larvae inblackflies2 Maintenance ofivermectin distributionEnsure high coverage cost-effectiveness andsustainable delivery viacommunity assisted byNGOs Ivermectinavailability free of charge
As 2 above but unlikelyto make major impact
As 2 above but unlikely tomake major impact
Ivermectin controlembarked upon
and socio-economic importance in seven countries (BeninBurkina Faso Cote dlvoire Ghana Mali Niger and Togo)of West Africa In 1986 the programme began operationsin an additional four countries in the West (Guinea GuineaBissau Senegal and Sierra Leone) and extended operationsinto the South and South-east in Benin Ghana and TogoThe rationale for these extensions related to findings thatSimulium were able to migrate and hence re-invadecontrolled areas over several hundred kilometres (Garmset al 1979)
The control strategy of the OCP was based on weeklyaerial larviciding of all breeding sites in the rivers of the
programme area using the organophosphate temephos(Abate) an insecticide with limited toxicity to non-targetaquatic fauna Larviciding would prevent emergence ofany adult flies and hence eliminate transmission of theparasite (O volvulus) It was proposed that aeriallarviciding should be continued for a period initiallyestimated at 20 years which was the maximum durationof life of the adult worm Recent detailed investigationsbased on field studies and supported by model predictionssuggest a reproductive life span of adult worms of 9-12years (Habbema et al 1992) Transmission of third-stagelarvae (L3) to humans with the resultant cessation of
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Epidemiology and control of onchocerciasis in West Africa 93
sevenlarvicides Emphasis on
fty-based distributionof ivermectinnsion of Ecological
Burkino Faso Cote dlvoireGhana Mali Niger Togo)
tor twenty years (expected
1968 1970 1973 1974 1975 1978-89 1980 1981 1983-85 1984 1985 1986 1988
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I1992 1994 1995 1996
Governanceand
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Fig 1 History and evolution of control strategy development in the Onchocerciasis Control Programme
recruitment of adults into the human population occurredwhen larviciding commenced In the absence of a non-toxic drug which could be used on a wide scale whichwould kill the adult worm transmission control was theonly strategy to deal with such an extensive public healthproblem which had become a major impediment todevelopment The OCP has evolved rapidly bothmanagerially and technically over the last 22 years (Samba1994) The changes which have taken place are outlinedin fig 1 which emphasizes the evolution of the OCP inresponse to both technical needs scientific advances andparticipating and donor country policies These changesand the effects of control have resulted in a situation ofenhanced complexity both in terms of epidemiology onthe one hand and control strategy on the other respectingthe need to bring the OCP to a successful conclusion tosafeguard public health achievements and ensure theirsustainability This need in 1990 led to the expansion ofthe Programme Objective to incorporate the statement toensure the countries are in a position to maintain thatachievement referring to the need to devolveresponsibility for post-OCP activities for onchocerciasissurveillance and control to appropriate national healthsystems This has been facilitated by the widespread useof ivermectin (Mectizanreg) which became an integral partof OCP control strategy in the late 1980s (Webbe 1992) Atpresent in the OCP area some 35 million tablets aredistributed annually to 25 million individuals The adventof ivermectin based control has had a significant impacton control strategy through the generosity of themanufacturer Merck and Co in providing the drug freefor the control of onchocerciasis The OCP control strategyhas evolved in response to key applied research findingsIn addition a continuous search for more cost-effectiveapproaches to control in a programme which expends a
high proportion of its costs on aerial larviciding (C 65-70 of $17m budget for 1998) The length of the riversystems under control have been reduced from the peakof 50000 km over an area of 12m km2 in the mid 1980s toa planned level in the last year of the 4th phase of theOCP in 1997 to 12000 km in an area of 600000 km2 Theprojected lengths of rivers treated in the final year of theprogramme will be 8000 km over an area of 400000 km2
The OCP has been subjected to extensive external reviewin order to reassure the donor community of the validity ofthe approaches to control (Webbe 1992 Molyneux 1995)whilst Samba (1994) has recorded the importance of theOCPs experience in the context of public healthmanagement issues There have been in addition reviewsof 10 years of onchocerciasis control (WHO 1985) and amonograph (O-Now Leiden 1990) which included manypapers emanating from OCP activities and recently theoverview of 20 years of onchocerciasis control (WHO 1997)The recent WHO Expert Committee Report (WHO 1995)summarizes all aspects of onchocerciasis control on the basisnot only of OCP experiences but on opportunities forivermectin-based control outside OCP in Africa as well asSouth and Central American foci The utilization ofivermectin as a tool to control onchocerciasis morbidity hasresulted in the establishment of a new programme theAfrican Programme for Onchocerciasis Control (APOC)APOC seeks to establish sustainable community-directedivermectin delivery systems in the non-OCP endemiccountries of Africa (Remme 1995) The programme is overa 12 year period through joint government and non-governmental development organization (NGDO)partnerships which will operate in-country via nationalOnchocerciasis Task Forces each community-directedtreatment project will be designed to achieve sustainabledelivery of ivermectin after 5 years programme support
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94 B Boatin et al
Table 2 Epidemiological entomological ophthalmological and ivermectin distribution OCP performance indicators
Vector controlNumbers of flies caught at capture points within areas under larviriding (biting rate) in standard timeNumbers of L3 of Onchocerca volvulus per head in flies caught according to above modalities (transmission potential)Numbers of infected flies per 1000 parous flies up to 2 years after cessation of larviciding (post-control studies)Level of susceptibility of flies to larvicides as indicators of the effectiveness of insecticide rotation system
- Increase cost-effectiveness of treatment using rotational systems as measured by reduced larvicide use and number of flyinghours against budgeted predictionMaintenance of quality control systems to evaluate the efficacy of insecticides
Epidemiological- Prevalence as determined by skin-snip as indicator in sentinel villages compared with pre-control prevalence (60) Objective
0 prevalence after 12 years controlTrends in the decline of prevalence over 12 years of controlCommunity microfilarial load in different situations against pre-control data after 12 years controlIncidence (a) no incidence in children born since vector control commenced in indicator villages (b) reduced incidence inchildren born since ivermectin first distributed in areas of ivermectin control alone compatible with no risk of increasedblindness in children annual transmission potentials (ATPs) at historic capture points Objective ATP lt100 compatible withno risk of blindness compared with pre-control ATPs Objective - zero incidence as a result of no transmission
Ophthalmological vector control combined with ivermectin controlNo risk of blindness in children born since programme beganRegression of anterior segment lesions Sclerosing keratitis iridocyclitisStabilization of posterior-segment lesions regression in optic nerve diseaseMaintenance of ophthalmological evaluation in selected villages
Ivermectin distributionNumbers of villages andor communities covered in areas under control to provide village coverage (objective 100)Coverage of population and treatment of all eligiblesMonitoring trend towards community-directed treatment from mobile team distribution with objective of at least 80coverage by community-directed approach by 1998 and 100 by the middle of 1999
- Maintenance of coverage and compliance rates over time- Regularity of treatment in conformity with expected frequency
Effective reporting of adverse reactionsHealth education has quantitative impact on coverage compliance and sensitization
The OCP was established to control onchocerciasis inthe West African savanna belt where the disease causedmassive depopulation and migration from river valleysprevented access to fertile alluvial river basins and in somevillages caused up to 30 of adults in communities to beblind and unable to work providing an increased burdenon already impoverished rural communities Whilst theeffects of blindness can be quantified more easily in termsof social and economic consequences of the burden on thehousehold the impact of other symptoms such as itchingare only recently being scrutinized It is clear from initialresults that there is an important psychosocial andeconomic dimension of onchocercal skin disease as yetunquantified (WHO 1995) but which assumes muchimportance to afflicted individuals who feel and arestigmatized
The OCP has consistently planned its activities on anannual basis and submitted detailed plans of operationsfor the various financial phases The final phase of theoperational plan (1998-2002) has been developedfollowing a review of OCP activities (see Molyneux 1995)and this included extensive discussions on trends in theprevalence incidence levels of community microfilarialload (CMFL) ophthalmological changes in the presenceof control annual transmission potentials (ATP) andnumbers of infective L31000 parous females proportionof O volvulus v O ochengi L3 in fly populations indicatingthe degree of zoophily (animal feeding) and proximity toinvading fly populations outside the boundaries of thecontrol programme (eg Nigeria south of OCP border)
Table 2 provides a list of indicators which determine thedecisions to be made on approaches to control
The different control situations and epidemiologicalcharacteristics are indicated in fig 2 The pre-controlindicators of the annual transmission potential andprevalence of skin microfilaria throughout the programmearea are compared with the current situation in figs 3aampband 4aampb The existing distribution of ivermectin is shownin fig 5
Control strategy
Area 1 Western extension
Senegal western Mali northern Guinea Guinea Bissau
In this area morbidity control is by ivermectin deliveryeither annually or biannually The rationale for only usingivermectin to control disease is that endemicity is low andalthough prevalence could be high the intensity ofinfection as judged by CMFLs is low Whilst transmissionis by savanna blackflies their migration does not pose anythreat to the original OCP area Annual transmissionpotential estimates were initially flawed as a result of highlevels of zoophily in Simulium as the L3 were often Oochengi (Trees 1992) Molecular identification shows 60of L3 are O ochengi in S sirbanumS damnosum Blindnessdue to Onchocerca was a limited public health problem ina sparsely populated area Recent epidemiological studiesindicate that even in the absence of larviciding an
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96 B Boatin et al
(a) Original OCP area (1973-1974)Southern extension (1978-1979)Western extension (1986-1989)
(b)
Simulium damnosum complex species infected with Onchocerca volvulus
n Entomological evaluation ceased as A Experimental entomological evaluation intrade from 1992 Results were excellent ATP = 0 w Bougouriba Partial ATP in 1995 is equal to 126Olt100
(3 100-1993 200-399 ~~bullmdashbullmdash- Boundary of the original OCP area
i pound 400-799 Northern and southern limit of larviciding in western extension
gt800 _ ^ _ mdash Programme limit
Fig 3 Annual transmission potentials pre-control (a) and in 1995(b)
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Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
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Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
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100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
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Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
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92 B Boatin et al
Table 1 Stratification of global onchocerciasis epidemiology and control
Geographical locality
AfricaSouth of SaharaOnchocerciasis ControlProgramme (OCP)countries
1 Original areas - BeninBurkina Faso Cotedlvoire Ghana MaliNiger Togo2 Extension areasSouthern areas of GhanaTogo Benin westernextension Guinea GuineaBissau Sierra LeoneSenegal
Non-OCP countries3 Nigeria to Sudan4 West and EquatorialAfrica Guinea-Bissau toGabon Rain forest5 Zaire Basin6 East Africa highlandsEthiopia to SouthernMalawi
Central AmericaGuatemala Mexico inwell defined foci Crossborder movement ofmigrant workers mayspread the disease
South America1 Brazil S Venezuela2 N Venezuela3 Ecuador Colombia
YemenDistributed along wadis
Epidemiological
Savannah woodland ofnorthern tropics Hyper-endemic villages close torivers Historicallyassociated with highblindness rate resultingin depopulation
Major vectors in savannaS damnosum and Ssirbanum Annualtransmission potential ormore than 100 associatedwith blindness riskHighly migratory
In forest areas lessblinding form of Ovolvulus transmitted byforest vectors S soubrenseS yahense S sanctipauli Ssquamosum S leonense(Sierra Leone) which areless efficient and non orless migratory
Anthropophilic Sochraceum in highlandfoci S metallicum morezoophilicalso involvedInefficiencyas vectordue to buccal armaturecomplicated byabundance
1 Primary vectors Soyapockense and Sguianense2 Primary vector Smetallicum3 Primary vector Sexiguum12 Secondary vector Sexiguum
A member of the Sdamnosum complex
Operational
1 Vector control byweekly aerial larvicidingfor 14 years eliminatesadult worms in humanreservoir Ivermectin forrecrudescence orundetected foci2 Combined vectorcontrol and ivermectin for12 years projected toreduce disease to non-significant levelIvermectin alone in areasof low CMFL (lt10) whereno invasion ofSimulium threatensoriginal OCP area345 Ivermectin throughcommunity baseddistribution systems6 or 3-5 Focal vectorcontrol could achieveeradication of S damnosumor S neavei
Control by ivermectindistribution via nationalprogrammes throughtwice yearly distribution
Vector control not feasibleIntegration of ivermectinwith other programmes
Control initiated
Disease management
1 Vector control applieddue to lack of availabilityof drug for large scaleuse till 1986 Thereafterivermectin to reduceinfection and preventdevelopment of ocularlesions2 Ivermectin throughoutfor extended periods upto 20 years as ivermectindoes not interrupttransmission3 Impact of ivermectin onskin disease and othermanifestations of Ovolvulus infection to beassessed
Ivermectin based
Ivermectin based
Ivermectin based
Prevention
1 Maintain surveillancesystem for recrudescenceusing tests for earlydetection of transmissionInstitute ivermectin ifappropriate Establishappropriate surveillancevia integration inpublic health systemsPossible detection of earlytransmission by detectionof infective larvae inblackflies2 Maintenance ofivermectin distributionEnsure high coverage cost-effectiveness andsustainable delivery viacommunity assisted byNGOs Ivermectinavailability free of charge
As 2 above but unlikelyto make major impact
As 2 above but unlikely tomake major impact
Ivermectin controlembarked upon
and socio-economic importance in seven countries (BeninBurkina Faso Cote dlvoire Ghana Mali Niger and Togo)of West Africa In 1986 the programme began operationsin an additional four countries in the West (Guinea GuineaBissau Senegal and Sierra Leone) and extended operationsinto the South and South-east in Benin Ghana and TogoThe rationale for these extensions related to findings thatSimulium were able to migrate and hence re-invadecontrolled areas over several hundred kilometres (Garmset al 1979)
The control strategy of the OCP was based on weeklyaerial larviciding of all breeding sites in the rivers of the
programme area using the organophosphate temephos(Abate) an insecticide with limited toxicity to non-targetaquatic fauna Larviciding would prevent emergence ofany adult flies and hence eliminate transmission of theparasite (O volvulus) It was proposed that aeriallarviciding should be continued for a period initiallyestimated at 20 years which was the maximum durationof life of the adult worm Recent detailed investigationsbased on field studies and supported by model predictionssuggest a reproductive life span of adult worms of 9-12years (Habbema et al 1992) Transmission of third-stagelarvae (L3) to humans with the resultant cessation of
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Epidemiology and control of onchocerciasis in West Africa 93
sevenlarvicides Emphasis on
fty-based distributionof ivermectinnsion of Ecological
Burkino Faso Cote dlvoireGhana Mali Niger Togo)
tor twenty years (expected
1968 1970 1973 1974 1975 1978-89 1980 1981 1983-85 1984 1985 1986 1988
I I I I I I I I I I I I I1989 1990 1991
I1992 1994 1995 1996
Governanceand
management MTunis meeting
discussesonchocerciasiscontrol in West
Africa andrecommendsProgramme
Establish menof
PrepatoryAssistance tltGovernment i
mission(PAG)
IndependentCommission
recommends needfor devolution and
onchocerciasischemotherapy project
later MACROFIL
JPC agreesto Western
and SouthernExtensions
Signingof OCP
Agreement
JPC approvesPlan of
Operations(1986-1991)
U5AID impactassessment
External Reviewconfirms strategy
appropriateto bring
Programmeto successful
conclusion
Mid-TermReview endorses
controlapproach anddefines OCPresponsibilityfor devolution
OCPandTDR
contributeto
launchingAPOC
JPCapprovesPlan of
Operations(1992-1997)
Fig 1 History and evolution of control strategy development in the Onchocerciasis Control Programme
recruitment of adults into the human population occurredwhen larviciding commenced In the absence of a non-toxic drug which could be used on a wide scale whichwould kill the adult worm transmission control was theonly strategy to deal with such an extensive public healthproblem which had become a major impediment todevelopment The OCP has evolved rapidly bothmanagerially and technically over the last 22 years (Samba1994) The changes which have taken place are outlinedin fig 1 which emphasizes the evolution of the OCP inresponse to both technical needs scientific advances andparticipating and donor country policies These changesand the effects of control have resulted in a situation ofenhanced complexity both in terms of epidemiology onthe one hand and control strategy on the other respectingthe need to bring the OCP to a successful conclusion tosafeguard public health achievements and ensure theirsustainability This need in 1990 led to the expansion ofthe Programme Objective to incorporate the statement toensure the countries are in a position to maintain thatachievement referring to the need to devolveresponsibility for post-OCP activities for onchocerciasissurveillance and control to appropriate national healthsystems This has been facilitated by the widespread useof ivermectin (Mectizanreg) which became an integral partof OCP control strategy in the late 1980s (Webbe 1992) Atpresent in the OCP area some 35 million tablets aredistributed annually to 25 million individuals The adventof ivermectin based control has had a significant impacton control strategy through the generosity of themanufacturer Merck and Co in providing the drug freefor the control of onchocerciasis The OCP control strategyhas evolved in response to key applied research findingsIn addition a continuous search for more cost-effectiveapproaches to control in a programme which expends a
high proportion of its costs on aerial larviciding (C 65-70 of $17m budget for 1998) The length of the riversystems under control have been reduced from the peakof 50000 km over an area of 12m km2 in the mid 1980s toa planned level in the last year of the 4th phase of theOCP in 1997 to 12000 km in an area of 600000 km2 Theprojected lengths of rivers treated in the final year of theprogramme will be 8000 km over an area of 400000 km2
The OCP has been subjected to extensive external reviewin order to reassure the donor community of the validity ofthe approaches to control (Webbe 1992 Molyneux 1995)whilst Samba (1994) has recorded the importance of theOCPs experience in the context of public healthmanagement issues There have been in addition reviewsof 10 years of onchocerciasis control (WHO 1985) and amonograph (O-Now Leiden 1990) which included manypapers emanating from OCP activities and recently theoverview of 20 years of onchocerciasis control (WHO 1997)The recent WHO Expert Committee Report (WHO 1995)summarizes all aspects of onchocerciasis control on the basisnot only of OCP experiences but on opportunities forivermectin-based control outside OCP in Africa as well asSouth and Central American foci The utilization ofivermectin as a tool to control onchocerciasis morbidity hasresulted in the establishment of a new programme theAfrican Programme for Onchocerciasis Control (APOC)APOC seeks to establish sustainable community-directedivermectin delivery systems in the non-OCP endemiccountries of Africa (Remme 1995) The programme is overa 12 year period through joint government and non-governmental development organization (NGDO)partnerships which will operate in-country via nationalOnchocerciasis Task Forces each community-directedtreatment project will be designed to achieve sustainabledelivery of ivermectin after 5 years programme support
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94 B Boatin et al
Table 2 Epidemiological entomological ophthalmological and ivermectin distribution OCP performance indicators
Vector controlNumbers of flies caught at capture points within areas under larviriding (biting rate) in standard timeNumbers of L3 of Onchocerca volvulus per head in flies caught according to above modalities (transmission potential)Numbers of infected flies per 1000 parous flies up to 2 years after cessation of larviciding (post-control studies)Level of susceptibility of flies to larvicides as indicators of the effectiveness of insecticide rotation system
- Increase cost-effectiveness of treatment using rotational systems as measured by reduced larvicide use and number of flyinghours against budgeted predictionMaintenance of quality control systems to evaluate the efficacy of insecticides
Epidemiological- Prevalence as determined by skin-snip as indicator in sentinel villages compared with pre-control prevalence (60) Objective
0 prevalence after 12 years controlTrends in the decline of prevalence over 12 years of controlCommunity microfilarial load in different situations against pre-control data after 12 years controlIncidence (a) no incidence in children born since vector control commenced in indicator villages (b) reduced incidence inchildren born since ivermectin first distributed in areas of ivermectin control alone compatible with no risk of increasedblindness in children annual transmission potentials (ATPs) at historic capture points Objective ATP lt100 compatible withno risk of blindness compared with pre-control ATPs Objective - zero incidence as a result of no transmission
Ophthalmological vector control combined with ivermectin controlNo risk of blindness in children born since programme beganRegression of anterior segment lesions Sclerosing keratitis iridocyclitisStabilization of posterior-segment lesions regression in optic nerve diseaseMaintenance of ophthalmological evaluation in selected villages
Ivermectin distributionNumbers of villages andor communities covered in areas under control to provide village coverage (objective 100)Coverage of population and treatment of all eligiblesMonitoring trend towards community-directed treatment from mobile team distribution with objective of at least 80coverage by community-directed approach by 1998 and 100 by the middle of 1999
- Maintenance of coverage and compliance rates over time- Regularity of treatment in conformity with expected frequency
Effective reporting of adverse reactionsHealth education has quantitative impact on coverage compliance and sensitization
The OCP was established to control onchocerciasis inthe West African savanna belt where the disease causedmassive depopulation and migration from river valleysprevented access to fertile alluvial river basins and in somevillages caused up to 30 of adults in communities to beblind and unable to work providing an increased burdenon already impoverished rural communities Whilst theeffects of blindness can be quantified more easily in termsof social and economic consequences of the burden on thehousehold the impact of other symptoms such as itchingare only recently being scrutinized It is clear from initialresults that there is an important psychosocial andeconomic dimension of onchocercal skin disease as yetunquantified (WHO 1995) but which assumes muchimportance to afflicted individuals who feel and arestigmatized
The OCP has consistently planned its activities on anannual basis and submitted detailed plans of operationsfor the various financial phases The final phase of theoperational plan (1998-2002) has been developedfollowing a review of OCP activities (see Molyneux 1995)and this included extensive discussions on trends in theprevalence incidence levels of community microfilarialload (CMFL) ophthalmological changes in the presenceof control annual transmission potentials (ATP) andnumbers of infective L31000 parous females proportionof O volvulus v O ochengi L3 in fly populations indicatingthe degree of zoophily (animal feeding) and proximity toinvading fly populations outside the boundaries of thecontrol programme (eg Nigeria south of OCP border)
Table 2 provides a list of indicators which determine thedecisions to be made on approaches to control
The different control situations and epidemiologicalcharacteristics are indicated in fig 2 The pre-controlindicators of the annual transmission potential andprevalence of skin microfilaria throughout the programmearea are compared with the current situation in figs 3aampband 4aampb The existing distribution of ivermectin is shownin fig 5
Control strategy
Area 1 Western extension
Senegal western Mali northern Guinea Guinea Bissau
In this area morbidity control is by ivermectin deliveryeither annually or biannually The rationale for only usingivermectin to control disease is that endemicity is low andalthough prevalence could be high the intensity ofinfection as judged by CMFLs is low Whilst transmissionis by savanna blackflies their migration does not pose anythreat to the original OCP area Annual transmissionpotential estimates were initially flawed as a result of highlevels of zoophily in Simulium as the L3 were often Oochengi (Trees 1992) Molecular identification shows 60of L3 are O ochengi in S sirbanumS damnosum Blindnessdue to Onchocerca was a limited public health problem ina sparsely populated area Recent epidemiological studiesindicate that even in the absence of larviciding an
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96 B Boatin et al
(a) Original OCP area (1973-1974)Southern extension (1978-1979)Western extension (1986-1989)
(b)
Simulium damnosum complex species infected with Onchocerca volvulus
n Entomological evaluation ceased as A Experimental entomological evaluation intrade from 1992 Results were excellent ATP = 0 w Bougouriba Partial ATP in 1995 is equal to 126Olt100
(3 100-1993 200-399 ~~bullmdashbullmdash- Boundary of the original OCP area
i pound 400-799 Northern and southern limit of larviciding in western extension
gt800 _ ^ _ mdash Programme limit
Fig 3 Annual transmission potentials pre-control (a) and in 1995(b)
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Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
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_ O
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Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
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100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
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Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
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Epidemiology and control of onchocerciasis in West Africa 93
sevenlarvicides Emphasis on
fty-based distributionof ivermectinnsion of Ecological
Burkino Faso Cote dlvoireGhana Mali Niger Togo)
tor twenty years (expected
1968 1970 1973 1974 1975 1978-89 1980 1981 1983-85 1984 1985 1986 1988
I I I I I I I I I I I I I1989 1990 1991
I1992 1994 1995 1996
Governanceand
management MTunis meeting
discussesonchocerciasiscontrol in West
Africa andrecommendsProgramme
Establish menof
PrepatoryAssistance tltGovernment i
mission(PAG)
IndependentCommission
recommends needfor devolution and
onchocerciasischemotherapy project
later MACROFIL
JPC agreesto Western
and SouthernExtensions
Signingof OCP
Agreement
JPC approvesPlan of
Operations(1986-1991)
U5AID impactassessment
External Reviewconfirms strategy
appropriateto bring
Programmeto successful
conclusion
Mid-TermReview endorses
controlapproach anddefines OCPresponsibilityfor devolution
OCPandTDR
contributeto
launchingAPOC
JPCapprovesPlan of
Operations(1992-1997)
Fig 1 History and evolution of control strategy development in the Onchocerciasis Control Programme
recruitment of adults into the human population occurredwhen larviciding commenced In the absence of a non-toxic drug which could be used on a wide scale whichwould kill the adult worm transmission control was theonly strategy to deal with such an extensive public healthproblem which had become a major impediment todevelopment The OCP has evolved rapidly bothmanagerially and technically over the last 22 years (Samba1994) The changes which have taken place are outlinedin fig 1 which emphasizes the evolution of the OCP inresponse to both technical needs scientific advances andparticipating and donor country policies These changesand the effects of control have resulted in a situation ofenhanced complexity both in terms of epidemiology onthe one hand and control strategy on the other respectingthe need to bring the OCP to a successful conclusion tosafeguard public health achievements and ensure theirsustainability This need in 1990 led to the expansion ofthe Programme Objective to incorporate the statement toensure the countries are in a position to maintain thatachievement referring to the need to devolveresponsibility for post-OCP activities for onchocerciasissurveillance and control to appropriate national healthsystems This has been facilitated by the widespread useof ivermectin (Mectizanreg) which became an integral partof OCP control strategy in the late 1980s (Webbe 1992) Atpresent in the OCP area some 35 million tablets aredistributed annually to 25 million individuals The adventof ivermectin based control has had a significant impacton control strategy through the generosity of themanufacturer Merck and Co in providing the drug freefor the control of onchocerciasis The OCP control strategyhas evolved in response to key applied research findingsIn addition a continuous search for more cost-effectiveapproaches to control in a programme which expends a
high proportion of its costs on aerial larviciding (C 65-70 of $17m budget for 1998) The length of the riversystems under control have been reduced from the peakof 50000 km over an area of 12m km2 in the mid 1980s toa planned level in the last year of the 4th phase of theOCP in 1997 to 12000 km in an area of 600000 km2 Theprojected lengths of rivers treated in the final year of theprogramme will be 8000 km over an area of 400000 km2
The OCP has been subjected to extensive external reviewin order to reassure the donor community of the validity ofthe approaches to control (Webbe 1992 Molyneux 1995)whilst Samba (1994) has recorded the importance of theOCPs experience in the context of public healthmanagement issues There have been in addition reviewsof 10 years of onchocerciasis control (WHO 1985) and amonograph (O-Now Leiden 1990) which included manypapers emanating from OCP activities and recently theoverview of 20 years of onchocerciasis control (WHO 1997)The recent WHO Expert Committee Report (WHO 1995)summarizes all aspects of onchocerciasis control on the basisnot only of OCP experiences but on opportunities forivermectin-based control outside OCP in Africa as well asSouth and Central American foci The utilization ofivermectin as a tool to control onchocerciasis morbidity hasresulted in the establishment of a new programme theAfrican Programme for Onchocerciasis Control (APOC)APOC seeks to establish sustainable community-directedivermectin delivery systems in the non-OCP endemiccountries of Africa (Remme 1995) The programme is overa 12 year period through joint government and non-governmental development organization (NGDO)partnerships which will operate in-country via nationalOnchocerciasis Task Forces each community-directedtreatment project will be designed to achieve sustainabledelivery of ivermectin after 5 years programme support
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94 B Boatin et al
Table 2 Epidemiological entomological ophthalmological and ivermectin distribution OCP performance indicators
Vector controlNumbers of flies caught at capture points within areas under larviriding (biting rate) in standard timeNumbers of L3 of Onchocerca volvulus per head in flies caught according to above modalities (transmission potential)Numbers of infected flies per 1000 parous flies up to 2 years after cessation of larviciding (post-control studies)Level of susceptibility of flies to larvicides as indicators of the effectiveness of insecticide rotation system
- Increase cost-effectiveness of treatment using rotational systems as measured by reduced larvicide use and number of flyinghours against budgeted predictionMaintenance of quality control systems to evaluate the efficacy of insecticides
Epidemiological- Prevalence as determined by skin-snip as indicator in sentinel villages compared with pre-control prevalence (60) Objective
0 prevalence after 12 years controlTrends in the decline of prevalence over 12 years of controlCommunity microfilarial load in different situations against pre-control data after 12 years controlIncidence (a) no incidence in children born since vector control commenced in indicator villages (b) reduced incidence inchildren born since ivermectin first distributed in areas of ivermectin control alone compatible with no risk of increasedblindness in children annual transmission potentials (ATPs) at historic capture points Objective ATP lt100 compatible withno risk of blindness compared with pre-control ATPs Objective - zero incidence as a result of no transmission
Ophthalmological vector control combined with ivermectin controlNo risk of blindness in children born since programme beganRegression of anterior segment lesions Sclerosing keratitis iridocyclitisStabilization of posterior-segment lesions regression in optic nerve diseaseMaintenance of ophthalmological evaluation in selected villages
Ivermectin distributionNumbers of villages andor communities covered in areas under control to provide village coverage (objective 100)Coverage of population and treatment of all eligiblesMonitoring trend towards community-directed treatment from mobile team distribution with objective of at least 80coverage by community-directed approach by 1998 and 100 by the middle of 1999
- Maintenance of coverage and compliance rates over time- Regularity of treatment in conformity with expected frequency
Effective reporting of adverse reactionsHealth education has quantitative impact on coverage compliance and sensitization
The OCP was established to control onchocerciasis inthe West African savanna belt where the disease causedmassive depopulation and migration from river valleysprevented access to fertile alluvial river basins and in somevillages caused up to 30 of adults in communities to beblind and unable to work providing an increased burdenon already impoverished rural communities Whilst theeffects of blindness can be quantified more easily in termsof social and economic consequences of the burden on thehousehold the impact of other symptoms such as itchingare only recently being scrutinized It is clear from initialresults that there is an important psychosocial andeconomic dimension of onchocercal skin disease as yetunquantified (WHO 1995) but which assumes muchimportance to afflicted individuals who feel and arestigmatized
The OCP has consistently planned its activities on anannual basis and submitted detailed plans of operationsfor the various financial phases The final phase of theoperational plan (1998-2002) has been developedfollowing a review of OCP activities (see Molyneux 1995)and this included extensive discussions on trends in theprevalence incidence levels of community microfilarialload (CMFL) ophthalmological changes in the presenceof control annual transmission potentials (ATP) andnumbers of infective L31000 parous females proportionof O volvulus v O ochengi L3 in fly populations indicatingthe degree of zoophily (animal feeding) and proximity toinvading fly populations outside the boundaries of thecontrol programme (eg Nigeria south of OCP border)
Table 2 provides a list of indicators which determine thedecisions to be made on approaches to control
The different control situations and epidemiologicalcharacteristics are indicated in fig 2 The pre-controlindicators of the annual transmission potential andprevalence of skin microfilaria throughout the programmearea are compared with the current situation in figs 3aampband 4aampb The existing distribution of ivermectin is shownin fig 5
Control strategy
Area 1 Western extension
Senegal western Mali northern Guinea Guinea Bissau
In this area morbidity control is by ivermectin deliveryeither annually or biannually The rationale for only usingivermectin to control disease is that endemicity is low andalthough prevalence could be high the intensity ofinfection as judged by CMFLs is low Whilst transmissionis by savanna blackflies their migration does not pose anythreat to the original OCP area Annual transmissionpotential estimates were initially flawed as a result of highlevels of zoophily in Simulium as the L3 were often Oochengi (Trees 1992) Molecular identification shows 60of L3 are O ochengi in S sirbanumS damnosum Blindnessdue to Onchocerca was a limited public health problem ina sparsely populated area Recent epidemiological studiesindicate that even in the absence of larviciding an
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1W
este
rn E
xten
sion
S
eneg
al
Wes
tern
Mal
iN
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ern
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nea
and
Gui
nea
Bis
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Mor
bidi
ty c
ontr
ol w
ithiv
erm
ectin
onl
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TP
P
reco
ntro
l = 5
90La
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taP
RE
VA
LEN
CE
P
reco
ntro
l = (
18
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19
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Wes
tern
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on
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ther
n S
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Tem
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ry i
nter
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r co
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l due
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secu
rity
O
ngoi
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erm
ectin
dis
trib
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nA
TP
P
reco
ntro
l = 1
110
Late
st =
15
3P
RE
VA
LEN
CE
P
reco
ntro
l = (
656
- 8
76)
Late
st =
(30
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49
0)3
Wes
tern
Ext
ensi
on
Sou
ther
n S
ierr
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one
Mor
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ty c
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ol w
ithiv
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ectin
onl
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P
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ntro
l = 3
993
Late
st =
no
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PR
EV
ALE
NC
E
Pre
cont
rol =
(60
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88
5)La
test
= (
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43)
4W
este
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xten
sion
M
ali
Sou
ther
n G
uine
aco
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ned
cont
rol w
ithla
rvic
idin
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ectin
for
a to
tal p
erio
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at
leas
t 12
yea
rs
AT
P
Pre
cont
rol =
132
6La
test
= 2
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RE
VA
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CE
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ntro
l = (
612
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Late
st =
(5
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)
5S
outh
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Ext
ensi
on
Cot
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O
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ng c
ombi
ned
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ith la
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idin
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erm
ectin
A
TP
P
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ntro
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Late
st =
51
PR
EV
ALE
NC
E
Pre
cont
rol =
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87
4)La
test
= (
00
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Orig
inal
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s-F
ree
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E
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nce
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ial c
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AT
P
Pre
cont
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180
0La
test
= 0
PR
EV
ALE
NC
E
Pre
cont
rol =
(60
0 -
84
2)La
test
= (
00
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0)
Sou
ther
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xten
sion
B
enin
Tog
o G
hana
co
mbi
ned
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rol w
ithla
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ectin
for
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at
leas
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rs
AT
P
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0La
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reco
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test
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)
AT
P A
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l Tra
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on P
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tial
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RE
VA
LEN
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(M
inim
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Max
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Pre
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nce
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icro
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iae
as
Fig
2 O
pera
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l m
ap o
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e O
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s C
ontr
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e in
199
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met
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96 B Boatin et al
(a) Original OCP area (1973-1974)Southern extension (1978-1979)Western extension (1986-1989)
(b)
Simulium damnosum complex species infected with Onchocerca volvulus
n Entomological evaluation ceased as A Experimental entomological evaluation intrade from 1992 Results were excellent ATP = 0 w Bougouriba Partial ATP in 1995 is equal to 126Olt100
(3 100-1993 200-399 ~~bullmdashbullmdash- Boundary of the original OCP area
i pound 400-799 Northern and southern limit of larviciding in western extension
gt800 _ ^ _ mdash Programme limit
Fig 3 Annual transmission potentials pre-control (a) and in 1995(b)
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Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
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_ O
CP
bou
ndar
y
_
_ O
rigin
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rogr
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e ar
ea
Ext
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on b
ound
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Sta
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r
Iver
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ent
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5 Z
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Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
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100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
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94 B Boatin et al
Table 2 Epidemiological entomological ophthalmological and ivermectin distribution OCP performance indicators
Vector controlNumbers of flies caught at capture points within areas under larviriding (biting rate) in standard timeNumbers of L3 of Onchocerca volvulus per head in flies caught according to above modalities (transmission potential)Numbers of infected flies per 1000 parous flies up to 2 years after cessation of larviciding (post-control studies)Level of susceptibility of flies to larvicides as indicators of the effectiveness of insecticide rotation system
- Increase cost-effectiveness of treatment using rotational systems as measured by reduced larvicide use and number of flyinghours against budgeted predictionMaintenance of quality control systems to evaluate the efficacy of insecticides
Epidemiological- Prevalence as determined by skin-snip as indicator in sentinel villages compared with pre-control prevalence (60) Objective
0 prevalence after 12 years controlTrends in the decline of prevalence over 12 years of controlCommunity microfilarial load in different situations against pre-control data after 12 years controlIncidence (a) no incidence in children born since vector control commenced in indicator villages (b) reduced incidence inchildren born since ivermectin first distributed in areas of ivermectin control alone compatible with no risk of increasedblindness in children annual transmission potentials (ATPs) at historic capture points Objective ATP lt100 compatible withno risk of blindness compared with pre-control ATPs Objective - zero incidence as a result of no transmission
Ophthalmological vector control combined with ivermectin controlNo risk of blindness in children born since programme beganRegression of anterior segment lesions Sclerosing keratitis iridocyclitisStabilization of posterior-segment lesions regression in optic nerve diseaseMaintenance of ophthalmological evaluation in selected villages
Ivermectin distributionNumbers of villages andor communities covered in areas under control to provide village coverage (objective 100)Coverage of population and treatment of all eligiblesMonitoring trend towards community-directed treatment from mobile team distribution with objective of at least 80coverage by community-directed approach by 1998 and 100 by the middle of 1999
- Maintenance of coverage and compliance rates over time- Regularity of treatment in conformity with expected frequency
Effective reporting of adverse reactionsHealth education has quantitative impact on coverage compliance and sensitization
The OCP was established to control onchocerciasis inthe West African savanna belt where the disease causedmassive depopulation and migration from river valleysprevented access to fertile alluvial river basins and in somevillages caused up to 30 of adults in communities to beblind and unable to work providing an increased burdenon already impoverished rural communities Whilst theeffects of blindness can be quantified more easily in termsof social and economic consequences of the burden on thehousehold the impact of other symptoms such as itchingare only recently being scrutinized It is clear from initialresults that there is an important psychosocial andeconomic dimension of onchocercal skin disease as yetunquantified (WHO 1995) but which assumes muchimportance to afflicted individuals who feel and arestigmatized
The OCP has consistently planned its activities on anannual basis and submitted detailed plans of operationsfor the various financial phases The final phase of theoperational plan (1998-2002) has been developedfollowing a review of OCP activities (see Molyneux 1995)and this included extensive discussions on trends in theprevalence incidence levels of community microfilarialload (CMFL) ophthalmological changes in the presenceof control annual transmission potentials (ATP) andnumbers of infective L31000 parous females proportionof O volvulus v O ochengi L3 in fly populations indicatingthe degree of zoophily (animal feeding) and proximity toinvading fly populations outside the boundaries of thecontrol programme (eg Nigeria south of OCP border)
Table 2 provides a list of indicators which determine thedecisions to be made on approaches to control
The different control situations and epidemiologicalcharacteristics are indicated in fig 2 The pre-controlindicators of the annual transmission potential andprevalence of skin microfilaria throughout the programmearea are compared with the current situation in figs 3aampband 4aampb The existing distribution of ivermectin is shownin fig 5
Control strategy
Area 1 Western extension
Senegal western Mali northern Guinea Guinea Bissau
In this area morbidity control is by ivermectin deliveryeither annually or biannually The rationale for only usingivermectin to control disease is that endemicity is low andalthough prevalence could be high the intensity ofinfection as judged by CMFLs is low Whilst transmissionis by savanna blackflies their migration does not pose anythreat to the original OCP area Annual transmissionpotential estimates were initially flawed as a result of highlevels of zoophily in Simulium as the L3 were often Oochengi (Trees 1992) Molecular identification shows 60of L3 are O ochengi in S sirbanumS damnosum Blindnessdue to Onchocerca was a limited public health problem ina sparsely populated area Recent epidemiological studiesindicate that even in the absence of larviciding an
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1W
este
rn E
xten
sion
S
eneg
al
Wes
tern
Mal
iN
orth
ern
Gui
nea
and
Gui
nea
Bis
sau
Mor
bidi
ty c
ontr
ol w
ithiv
erm
ectin
onl
yA
TP
P
reco
ntro
l = 5
90La
test
= n
o da
taP
RE
VA
LEN
CE
P
reco
ntro
l = (
18
8-8
19
)La
test
= (
00
-17
0)
Wes
tern
Ext
ensi
on
Nor
ther
n S
ierr
a Le
one
Tem
pora
ry i
nter
rupt
ion
of v
ecto
r co
ntro
l due
to in
secu
rity
O
ngoi
ngiv
erm
ectin
dis
trib
utio
nA
TP
P
reco
ntro
l = 1
110
Late
st =
15
3P
RE
VA
LEN
CE
P
reco
ntro
l = (
656
- 8
76)
Late
st =
(30
4 -
49
0)3
Wes
tern
Ext
ensi
on
Sou
ther
n S
ierr
a Le
one
Mor
bidi
ty c
ontr
ol w
ithiv
erm
ectin
onl
yA
TP
P
reco
ntro
l = 3
993
Late
st =
no
data
PR
EV
ALE
NC
E
Pre
cont
rol =
(60
2 -
88
5)La
test
= (
390
- 7
43)
4W
este
rn E
xten
sion
M
ali
Sou
ther
n G
uine
aco
mbi
ned
cont
rol w
ithla
rvic
idin
giv
erm
ectin
for
a to
tal p
erio
d of
at
leas
t 12
yea
rs
AT
P
Pre
cont
rol =
132
6La
test
= 2
2P
RE
VA
LEN
CE
P
reco
ntro
l = (
612
- 8
26)
Late
st =
(5
0 -
238
)
5S
outh
ern
Ext
ensi
on
Cot
edlv
oire
O
ngoi
ng c
ombi
ned
cont
rol w
ith la
rvic
idin
giv
erm
ectin
A
TP
P
reco
ntro
l = 4
500
Late
st =
51
PR
EV
ALE
NC
E
Pre
cont
rol =
(49
4 -
87
4)La
test
= (
00
- 50
6)
Orig
inal
are
aO
ncho
cerc
iasi
s-F
ree
zone
E
pide
mio
logi
cal
surv
eilla
nce
in s
entin
el v
illag
es
a-f
in
dica
te f
oci u
nder
spec
ial c
onsi
dera
tion
AT
P
Pre
cont
rol =
180
0La
test
= 0
PR
EV
ALE
NC
E
Pre
cont
rol =
(60
0 -
84
2)La
test
= (
00
- 6
0)
Sou
ther
n E
xten
sion
B
enin
Tog
o G
hana
co
mbi
ned
cont
rol w
ithla
rvic
idin
giv
erm
ectin
for
a to
tal p
erio
d of
at
leas
t 12
yea
rs
AT
P
Pre
cont
rol =
990
0La
test
= 3
44P
RE
VA
LEN
CE
P
reco
ntro
l = (
60
4-8
51
)La
test
= (
14
0-6
45
)
AT
P A
nnua
l Tra
nsm
issi
on P
oten
tial
expr
esse
d as
mea
nP
RE
VA
LEN
CE
(M
inim
um -
Max
imum
) of
Pre
vale
nce
of m
icro
filar
iae
as
Fig
2 O
pera
tiona
l m
ap o
f th
e O
ncho
cerc
iasi
s C
ontr
ol P
rogr
amm
e in
199
6 c
ontr
ol s
trat
egy
and
epid
emio
logi
cal
para
met
ers
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96 B Boatin et al
(a) Original OCP area (1973-1974)Southern extension (1978-1979)Western extension (1986-1989)
(b)
Simulium damnosum complex species infected with Onchocerca volvulus
n Entomological evaluation ceased as A Experimental entomological evaluation intrade from 1992 Results were excellent ATP = 0 w Bougouriba Partial ATP in 1995 is equal to 126Olt100
(3 100-1993 200-399 ~~bullmdashbullmdash- Boundary of the original OCP area
i pound 400-799 Northern and southern limit of larviciding in western extension
gt800 _ ^ _ mdash Programme limit
Fig 3 Annual transmission potentials pre-control (a) and in 1995(b)
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Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
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_ O
CP
bou
ndar
y
_
_ O
rigin
al P
rogr
amm
e ar
ea
Ext
ensi
on b
ound
ary
Sta
te b
orde
r
Iver
mec
tin tr
eatm
ent
area
s
Fig
5 Z
ones
of
iver
mec
tin d
istr
ibut
ion
in t
he O
ncho
cerc
iasi
s C
ontr
ol P
rogr
amm
e ar
ea
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Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
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100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
1W
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Fig
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rogr
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e in
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and
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para
met
ers
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96 B Boatin et al
(a) Original OCP area (1973-1974)Southern extension (1978-1979)Western extension (1986-1989)
(b)
Simulium damnosum complex species infected with Onchocerca volvulus
n Entomological evaluation ceased as A Experimental entomological evaluation intrade from 1992 Results were excellent ATP = 0 w Bougouriba Partial ATP in 1995 is equal to 126Olt100
(3 100-1993 200-399 ~~bullmdashbullmdash- Boundary of the original OCP area
i pound 400-799 Northern and southern limit of larviciding in western extension
gt800 _ ^ _ mdash Programme limit
Fig 3 Annual transmission potentials pre-control (a) and in 1995(b)
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Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
_ O
CP
bou
ndar
y
_
_ O
rigin
al P
rogr
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e ar
ea
Ext
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on b
ound
ary
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te b
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r
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ent
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s
Fig
5 Z
ones
of
iver
mec
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ibut
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in t
he O
ncho
cerc
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s C
ontr
ol P
rogr
amm
e ar
ea
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
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100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
96 B Boatin et al
(a) Original OCP area (1973-1974)Southern extension (1978-1979)Western extension (1986-1989)
(b)
Simulium damnosum complex species infected with Onchocerca volvulus
n Entomological evaluation ceased as A Experimental entomological evaluation intrade from 1992 Results were excellent ATP = 0 w Bougouriba Partial ATP in 1995 is equal to 126Olt100
(3 100-1993 200-399 ~~bullmdashbullmdash- Boundary of the original OCP area
i pound 400-799 Northern and southern limit of larviciding in western extension
gt800 _ ^ _ mdash Programme limit
Fig 3 Annual transmission potentials pre-control (a) and in 1995(b)
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
_ O
CP
bou
ndar
y
_
_ O
rigin
al P
rogr
amm
e ar
ea
Ext
ensi
on b
ound
ary
Sta
te b
orde
r
Iver
mec
tin tr
eatm
ent
area
s
Fig
5 Z
ones
of
iver
mec
tin d
istr
ibut
ion
in t
he O
ncho
cerc
iasi
s C
ontr
ol P
rogr
amm
e ar
ea
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 97
(a)
(b)
Original OCP area (1974-1977)Southern extension Cote dlvoire (1979)
Western and Southern extensions (1987-1990)
Boundary of the original OCP area
1 Limit of western and southern extensions
Fig 4 Prevalence of skin microfilaiiae pre-control (a) and from 1993 to 1996(b)
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
_ O
CP
bou
ndar
y
_
_ O
rigin
al P
rogr
amm
e ar
ea
Ext
ensi
on b
ound
ary
Sta
te b
orde
r
Iver
mec
tin tr
eatm
ent
area
s
Fig
5 Z
ones
of
iver
mec
tin d
istr
ibut
ion
in t
he O
ncho
cerc
iasi
s C
ontr
ol P
rogr
amm
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ea
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
_ O
CP
bou
ndar
y
_
_ O
rigin
al P
rogr
amm
e ar
ea
Ext
ensi
on b
ound
ary
Sta
te b
orde
r
Iver
mec
tin tr
eatm
ent
area
s
Fig
5 Z
ones
of
iver
mec
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istr
ibut
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in t
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s C
ontr
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httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 99
ivermectin-alone strategy providing high coverage hasprevented any incidence of infection in the under-5population who qualify to receive ivermectin for the firsttime Recent studies in Guinea Bissau and Guinea show areduction in prevalence of 16-23 to 02-32 and 482-627 to 86-446 respectively results similar to thoseobserved in Senegal and North West Mali
Area 2 Western extension
Northern Sierra Leone
Due to security problems aerial larviciding of riversystems SeliBagbe and KabaMongo was suspended for2-4 years from 1992-1996 ivermectin distribution was alsosuspended over the period but recommenced in early 1996During 1995 it was found that the proportion of savannaflies was lower than originally found in these rivers butthis rose significantly between 1995 and 1996 it wasconsidered that larviciding must recommence to avoidproliferation of the savanna fly populations and preventreinvasion of river systems in adjacent Guinea In this areaepidemiological data indicated onchocerciasis was of theforest form but this required confirmation by molecularidentification Present ATPs in north Sierra Leone are stillconsistent with onchocerciasis being a public healthproblem (an ATP greater than 100) The prevalence ofinfection whilst still high is lower than the pre-controllevel and similar to what was obtained before treatmentwas suspended The strategy of intensive ivermectindistribution (twice yearly) and larviciding until 2002 isthe only available strategy with continued communitydirected distribution post 2002 The 2-4 year gap inlarviciding in these key areas will require the OCP to beaware of the implications further east as transmission bysavanna flies albeit at a lower level has continued tointroduce new infections in the population This areawould be an ideal region to introduce a macrofilaricide ifit was available
Area 3 Western extension
Southern Sierra Leone
In this area high ATPs and CMFLs were found althoughthe level of blindness observed and the severity of ocularmorbidity was not compatible with parasitological findingsor as severe as in classical savanna blinding onchocerciasis(Dadzie et al 1992 De Sole et al 19911993) Studies on thevectors indicated the presence of a new Simulhim speciesS leonense which has a remarkably high vectorial capacitybut transmits a less blinding form of O volvulus (Boakye etal 1993) Simuliunt leonense is a forest species with limitedmigratory capacity not seemingly capable of establishingitself outside its limited area of distribution of southernSierra Leone and Liberia The extensive and vast breedingsites used by S leonense in rivers such as the Sewa with oneof the highest discharges in West Africa would meanlarviciding which even if appropriate would be extremelyexpensive and S leonense in any case does not pose a threatto the original OCP area Control is therefore only feasibleby ivermectin which was begun in 1990 but suspended ayear later due to the unstable security situation
Area 4 Western extension
Mali southern Guinea
This area of the upper Niger basin has been subjectedto regular control by larviciding and annual ivermectindistribution in former hyper- and meso-endemic villagessince 19871989 This combined approach will continuefor a 12 year period To date there has been a more rapidreduction in ocular morbidity indicators compared withthe previous experience in core OCP areas whenivermectin was not available between 1974 and 1987whilst larviciding in these river systems has arrestedmigration of Simulium into the western parts of the initialOCP area There has been a rapid reduction of allepidemiological parameters (ATP CMFL prevalence)with no incidence in children under-5 born sincecontrol began and excluded from ivermectin treatmentOphthalmological evaluation after 7 years of ivermectintreatment and larvicidal control showed reductions in bothanterior segment (sclerosing keratitis - 37 reduction andiridocyclitis - 775 reduction) and posterior segment(optic nerve disease - 46 reduction) whilst the prevalenceof microfilariae in the eye was reduced over a 7 year periodfrom 216 to less than 17 The mean microfilarial loadin the anterior chamber is of the order of 01
Area 5 Southern extension in Cote dlvoire
This area has been subjected to larviciding in 1979 andregular ivermectin distribution since 1992 when it wasrecognized that savanna Simulium were breeding furthersouth than expected The area has also posed problemsdue to temephos insecticide resistance In some zonesoutside the OCP area in Cote dlvoire Lower Comoe andLower Sassandra deforestation has provided furtheropportunities for increased populations of savannacytospecies to colonize river systems thereby increasingthe capacity for transmission of savanna O volvulus in anarea where both forest and savanna forms of O volvulusare present This therefore makes the epidemiologycomplex a situation which is further exacerbated byextensive patterns of human migration
Area 6 South-east extension
Benin Togo Ghana
In this area the control by larviciding and ivermectindistribution is scheduled for a 12 year period since thecommencement of control in the late 1980s Similar changesin the epidemiological patterns (incidence CMFLprevalence ocular disease) have occurred to those in thewestern extension There is some infiltration of infectedflies from the eastern border where uncontrolled areas ofNigeria are reservoirs of infection Any threat to theprogramme area is mitigated by continuous ivermectindistribution in eastern border areas of the OkparaOuemeriver systems and the SotaAlibori river basin As insouthern areas of Cote dlvoire there are complexepidemiological patterns caused by a mix of severalcytospecies transmitting both forest and savannaOnchocerca In addition in some areas vector control is
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
100 B Boatin et al
difficult due to mountainous conditions (Oti PendjariAtacora regions) where many small streams act as breedingsites of both savanna flies and S squamosum These areascannot be effectively treated using helicopters and thevillages are difficult to access for ivermectin distributionbecause of the mountainous terrain
Area 7 Original programme area
Throughout this area onchocerciasis is no longer apublic health problem The areas identified below are thosesubjected to special interventions to reduce any long termrisk of recrudescence These are identified on fig 2 aspoints a-fa Kankelaba Mali In this area fly reinvasion from the
west occurred until 1989 when the extension areabecame under effective control in GuineaLarviciding and ivermectin treatment will continueuntil the epidemiological parameters are judgedsatisfactory
b Dienkoa area of Burkina Faso (Upper Black Volta)An unrecognized breeding site maintained a focus oftransmission during early phases of the OCRIvermectin distribution together with groundlarviciding (using temephos and Bacillus thuringiensisH14 toxin) are currently maintained The key indicatorto assess effectiveness of control in this area is theincidence of infection
c Bougouriba Basin Burkina Faso This area has beenthe subject of concern since 1995 when high prevalenceswere found in some villages which had shown anapparent rapid increase and spread of prevalenceover a period of 12 months Studies to ascertain thereason for and dynamics of this recrudescence areunderway The likely reasons are that unidentifiedbreeding sites remained as sources of flies afterexceptional hydrological conditions in the mid-1980snew breeding sites were created or that migration ofinfected individuals from outside the OCP occurredthis is unlikely as the settlement process was controlledby a national authority The dynamics of recrudescencein this area eg the extent of areas of high prevalencethe rate of spread and a comparison of the predicteddynamics of transmission on the basis of theONCHOSIM model (Habbema et al 1992 Plaisier1996) need to be compared with the observedchanges in epidemiological parameters to understandnot only the most appropriate modes of ivermectindelivery but also the frequency of treatment to reduceor arrest transmission
d Kulpawn and Mole river systems Ghana In thisregion some villages maintain a relatively highprevalence (10-20) despite low CMFLs somechildren have also been found infected despite 15+years of vector control A bi-annual distribution ofivermectin has been introduced in villages with highprevalences together with parallel epidemiologicalstudies
e South West Ghana Black Volta In areas around themajor breeding sites of the Black Volta transmissioncontrol has not been as effective as anticipated Howeverin the area south of Bui in the Tano river system southof the OCP border epidemiological studies are
underway to assess the prevalence of savannaonchocerciasis and the frequency of colonization ofsavanna blackflies in deforested areas in the Tano river
f Sota-Alibori area of north Benin The continuousinfiltration of infected blackflies from Nigeria hasallowed transmission to continue so that distributionof ivermectin every 6 months must be maintained asa control measure
As the OCP draws to a close it will need to closelymonitor areas where continuing special interventions willbe required using ivermectin distribution strategiesespecially in the OtiPendjari area Pru basin GhanaTinkissou basin in Guinea Control beyond the year 2002will be dependent upon the commitment of nationalresources and the efficacy of community-directedivermectin treatment programmes
Acknowledgements
Professor Molyneux is grateful for the earlyencouragement in his career from Donald Lee as wellas the opportunity to publish this paper with colleaguesin the Onchoceriasis Control Programme
References
Boakye DA Post RJ Mosha FW Surtees DP amp BakerRHA (1993) Cytotaxonomic revision of the Simuliumsanctipauli subcomplex (Diptera Simuliidae) in Guinea andthe adjacent countries including description of the two newspecies Bulletin of Entomological Research 83171-186
Crosskey RW (1987) A taxa summary for the Simuliumdamnosum complex with special reference to distributionoutside the control areas of West Africa Annals of TropicalMedicine and Parasitology 81181-192
Dadzie KY De Sole G amp Remme J (1992) Occularonchocerciasis and the intensity of infection in thecommunity IV The degraded forest of Sierra LeoneTropical Medicine and Parasitology 43 75-79
De Sole G Baker R Dadzie YD Giese J Guillet PKeita EM amp Remme J (1991) Onchocerciasisdistribution and severity in five West African countriesBulletin of the World Health Organization 69 689-698
De Sole G Accorsi A Creusvaux H Giese J Keita EMamp Remme J (1993) Distribution of onchocerciasis inselected river basins of four West African countriesTropical Medicine and Parasitology 44 159-164
Duke DOL Lewis DJ amp Moore PJ (1966) Onchocerca-Simulium complexes I Transmission of forest and Sudansavanna strains of Onchocerca volvulus from Cameroonby Simulium damnosum from various West Africanbioclimatic zones Annals of Tropical Medicine andParasitology 60 318-336
Garms R Walsh JE amp Davies JB (1979) Studies on thereinvasion of the Onchocerciasis Control Programme inthe Volta River basin by Simulium damnosum sl withemphasis on the south western areas Tropenmedizin undParasitologie 30 345-362
Habbema JDE Alley ES Plaisier AP Van OortmarssenGJ amp Remme JHE (1992) Epidemiological modellingfor Onchocerciasis control Parasitology Today 8 99-103
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at
Epidemiology and control of onchocerciasis in West Africa 101
Le Berre R Walsh JF Phillipon B Poudiougo PHenderickx JEE Guillet P Seketeli A QuillevereD Grunewald J amp Cheke RA (1990) TheOnchocerciasis Control Programme retrospect andprospects Philosophical Transactions of the Royal SocietyLondon B 328 721-729
Molyneux DH (1995) Onchocerciasis control in West Africacurrent status and future of the Onchocerciasis ControlProgramme Parasitology Today 11 399^102
O-Now (1990) Proceedings of the Symposium onOnchocerciasis Leiden The Netherlands 481 pp
Plaisier AP (1996) Modelling onchocerciasis transmissionand control 181 pp PhD thesis Erasmus UniversityRotterdam
Remme JHF (1995) The African Programme forOnchocerciasis Control preparing to launch ParasitologyToday 11 403-406
Samba EM (1994) The Onchocerciasis Control Programmein West Africa An example of effective public healthmanagement 107 pp WHO Geneva
Trees AJ (1992) Onchocerca ochengi mimic model ormodulator of O volvulus Parasitology Today 8 337-339
Webbe G (1992) The Onchocerciasis Control ProgrammeTransactions of the Royal Society of Tropical Medicine andHygiene 86 113-114
World Health Organization (1995) Onchocerciasis and itscontrol Report of a WHO Expert Committee Technical ReportSeries 852 103 pp
World Health Organization (1997) Twenty years ofonchocerciasis control in West Africa Review of the workthe Onchocerciasis Control Programme in West Africafrom 1974-1994 Published by the World HealthOrganization
Zimmerman PA Dadzie YD De Sole G Remme JAlley ES amp Unnasch TR (1992) Onchocerca volvulusDNA probe classification correlates withepidemiological patterns of blindess Journal of InfectiousDiseases 165 964-968
(Accepted 19 February 1997)copy CAB INTERNATIONAL 1997
httpswwwcambridgeorgcoreterms httpsdoiorg101017S0022149X00015741Downloaded from httpswwwcambridgeorgcore University of Basel Library on 11 Jul 2017 at 081414 subject to the Cambridge Core terms of use available at