Legon, GhanaFebruary 1999

Current concern regarding public healthissues and recent evidence suggestingthe animal origin of some human patho-gens, such as HIV-1 (Ref. 1) and newvariant CJD, have put zoonotic diseasesat the top of the agenda. In the UK, re-cent problems have arisen from newlyemerging strains or variants, such asVTEC E. coli, Salmonella typhimuriumdt104 and, of course, BSE. In developingcountries, zoonotic diseases are alsomajor causes of morbidity and mortality,but the most prevalent zoonoses, such asrabies, anthrax, brucellosis, tuberculosisand cysticercosis, are diseases for whicheffective control measures are well es-tablished in more-affluent countries. Themovement of people from rural tourban environments, and the corre-sponding expansion of peri-urban areas,where large numbers of people live inclose proximity to livestock, increasesthe risk of zoonotic disease. How devel-oping countries might improve the con-trol of zoonotic disease within existinginfrastructures was the topic of a recentmeeting in Ghana.

The Challenge of Zoonoses

Zoonoses are defined by WHO asinfections that are naturally transmittedbetween vertebrate animals and man, ofwhich 166 are currently recognized byWHO, encompassing a broad range ofagents, from viruses to macroparasites.Although the epidemiology, diagnosisand treatment will be specific to eachdisease, there are some common re-quirements for disease control. Highquality baseline data that indicate whichdiseases are the greatest causes of mor-bidity and mortality are essential to pri-oritize targets for disease control (P.Shears, Liverpool School of Tropical Medi-cine, UK). At present, there are fewlarge-scale surveillance schemes in WestAfrica to provide sufficient data to makeinformed choices. Reasons for this in-clude the lack of diagnostic capabilities,which result from poor infrastructureand lack of resources, combined with in-adequate disease reporting systems. Insuf-ficient collaboration and communicationbetween health and veterinary services

frequently contribute to the failure ofdisease outbreak reports to be dissemi-nated and acted upon (E. Oppong, Uni-versity of Ghana, Ghana). A representa-tive of the UK Public Health LaboratoryService, T. Coleman, emphasized theneed for good surveillance, using as anexample a recent scheme in the UK todetermine the extent of zoonotic dis-ease in farm workers. Pre-conceivedperceptions of the prevalence and inci-dence of zoonotic disease are oftenwrong, and previously unexpected as-sociations might exist between certainanimals and human disease.

Veterinarians have a slightly differentperspective of zoonoses (D. Clifford,CVL; P. Cripps, University of Liverpool,UK). Zoonoses, by definition, cause dis-ease in humans, but they also cause dis-ease and welfare problems in domesticanimals as well as economic losses fortheir owners. Veterinarians have a majorrole to play in the control of zoonosesthrough: (1) examination of animals im-ported into, or moved within, countries;(2) meat inspection and abattoir records;and (3) monitoring herd/flock health.Veterinarians can also provide early warn-ing for epidemics and emerging zoo-noses, however, as in the health services,there are difficulties within state veteri-nary services in diagnosis and reportingof zoonotic disease. Poor training forveterinary field workers, lack of trans-port and difficulties in treating animals of nomadic herdsmen compound theproblem of effective control.

Schemes used to control bovine tu-berculosis (TB) in affluent countries, ie.the identification and slaughter of infectedcattle with payment of compensation,are not realistic in many West AfricanStates (O. Bonsu, Veterinary Services,Ghana). Nevertheless, control of somezoonoses can and has been achieved ata local level. In Ghana, for example, asmall but successful scheme with farmerand community participation to minimizethe risks of contracting TB from nonpas-teurized milk, involves the local collec-tion and pasteurization of milk beforesale to retail outlets and milk-processingindustries. This government sponsoredscheme is successful because a premiumis paid to farmers for milk from Myco-bacterium bovis-free cattle. Prevalence ofM. bovis in cattle is 11.3–19.0% in the

Dangme-West District of Ghana, andBonsu noted that such schemes enablelocal veterinarians and health workers toinform people of the risks from drinkingnonpasteurized milk.

Regional Perspectives

Regional veterinary and medical rep-resentatives presented national per-spectives on the control of zoonoses. S.Sackey (Disease Control Unit, Ministryof Health, Ghana) highlighted what thePublic Health Service regards as thethree principal zoonoses in Ghana: yel-low fever, rabies and anthrax. In eachcase, the implementation of remedialcontrol measures could dramatically re-duce the number of cases, but often suchmeasures are applied inadequately. Of-ficial statistics suggest that anthrax hasclaimed over 1000 lives in Ghana since1980, resulting from sporadic outbreaks,but slow responses from the health andveterinary services and poor monitoringmeant they were inadequately contained.The theme of anthrax was continued byG. Opoku-Pare (Veterinary Services De-partment, Ghana) who noted that ani-mals are a valuable commodity and in-vestment for most West Africans, so thesudden death of cattle with no prospectof compensation can be financially dev-astating. Consumption of meat fromanthrax-infected animals or exhumationof animal carcasses for recovery of hides,contributes to the high correlation be-tween human and animal disease. Therehave been 76 reported outbreaks ofanthrax in animals in Ghana since 1994,but it was fully acknowledged that thisrepresents serious under-reporting. Theother principal zoonoses in Ghana, iden-tified by the Veterinary Services, includedTB, brucellosis and cysticercosis. J. Arko-Mensah and W. Van Der Puije (Uni-versity of Ghana, Ghana) reported onrecent surveys indicating the high sero-prevalance of toxoplasmosis in pigs andgoats in Ghana (up to 40%), but high-lighted the need to extend the investi-gation of toxoplasmosis into humanhealth. Insufficient resources often meansthat diseases making headlines in moreaffluent countries, such as toxoplas-mosis, E. coli, Salmonella, Campylobacter,Giardia and Cryptosporidium are not in-vestigated in West Africa.

Parasitology Today, vol. 15, no. 8, 1999 3090169-4758/99/$ – see front matter © 1999 Elsevier Science. All rights reserved. PII: S0169-4758(99)01488-X

News

Zoonoses in West Africa: Impact and Control

J.M. Wastling, B.D. Akanmori and D.J.L.Williams

Medical and veterinary experts fromBurkina Faso and Togo agreed with theexperiences of neighbouring countries,with anthrax, TB, rabies and yellow feverconsidered to be the most significantzoonoses. D. Amedeganato (Universitédu Benin, Togo) and R. Yameogo (Min-istry of Health, Burkino Faso) highlightedcysticercosis and toxoplasmosis (rapidlygaining importance because of reacti-vation during HIV infection) as two im-portant parasitic zoonoses. A.M. Domingo(Ministry of Agriculture, Togo) and N.Coulibaly [National Institute for Agricul-tural Research (INERA), Burkina Faso]presented substantial veterinary epidemio-logical data on brucellosis, cysticercosis,rabies and anthrax, but again highlightedthe problems of under-reporting, late re-porting and poor surveillance; a situationoften compounded by poor veterinarydiagnostic facilities.

The veterinary and medical expertsfrom each country often had a slightlydifferent perspective of which zoonoseswere most important. This might reflecta difference in how data were collected,ie. data for human disease were ob-tained primarily from hospital records;veterinarians used abattoir records orsurveys, where prevalence of infectionwas assessed on individual farms or vil-lages. Some striking features were ap-parent: (1) the incidence of TB in the hu-man population was rarely associated, inthe minds of the medical workers, withpossible exposure to cattle; however,the limited data available suggest that10% of human TB is due to M. bovis, andin some villages it might be as high as50% (D. Kambarage, Sokoine University,Tanzania). (2) Brucellosis was regardedas a major problem in veterinary species,particularly in small ruminants, yet therewas a lack of data for the human popu-lation throughout the region.

Linking Public Health andVeterinary Services

Nigeria, with a population of over100 million, has to deal with zoonoticdisease on a different scale to that of itsneighbours. A. Coker (College of Medi-cine, University of Lagos, Nigeria) re-viewed the annual incidence of endemiczoonoses of Nigeria, including rabies,trypanosomiasis, TB, yellow fever, toxo-plasmosis and Campylobacter. Zoonosesdo not respect national boundaries, there-fore, a co-ordinated regional approachusing a West African health informationsystem is required. Nigeria is unique inWest Africa in having five Schools ofVeterinary Medicine, and could play akey role in bringing together medical and

veterinary workers (R. Ezuegwu, NationalVeterinary Research Institute, Nigeria).However, the move to privatize vet-erinary services means that there arenow more private veterinary practition-ers than state ones in Nigeria. The pro-vision and responsibility of State veteri-nary services throughout the region ledto heated debate with many delegatessuggesting that the private sector is notlikely to provide the level of disease sur-veillance necessary for effective controlof zoonoses.

Public and ProfessionalAwareness

Questionnaire surveys (O. Bonsu, E.Otupiri, M. Tettey, School of PublicHealth, University of Ghana, Ghana) re-vealed that in some areas there is pooror non-existent awareness about dis-eases that can be transmitted from ani-mals to humans. When questioned,most people did not know the routes oftransmission of TB or that cattle couldpass disease on to humans. Even whenthe risk of disease is known, there re-mains the problem of compliance. Zoo-notic diseases like cysticercosis (preva-lence in Ghana 2–10% at slaughter) canbe prevented by inspection of meat. In Ghana, recent investment has dra-matically improved provision for meatinspection, but S. Sackey noted that fa-cilities are often under-used and thatslaughtering still occurs outside abat-toirs. Lack of knowledge, as well as fi-nancial considerations, leads to the per-ception that, for many, meat inspectionis an ‘optional extra’. Only strong po-litical will to enforce existing regulationsand better education of meat produc-ers and market traders will solve suchproblems.

Workshop Recommendations

Surveillance. Currently, none of thecountries represented felt they had suf-ficient knowledge about which zoonoticdiseases are either the most common, in terms of their prevalence or inci-dence, or the most significant, in termsof the social and economic impact. Allthe data presented here were derivedfrom hospital records, abattoir surveysor small-scale ad hoc studies. There is aneed for data from high quality surveil-lance schemes, which would enable coun-tries to set priorities for disease control,using limited resources to their fullesteffect. Once a baseline has been set forthe most important diseases, then con-tinuing surveillance would monitor theeffectiveness of any control scheme,

warn of re-emergence of existing diseaseand detect newly emerging diseases. Togain full value from surveillance, systemsfor reporting and disseminating infor-mation nationally and regionally need tobe optimized in the context of integratednational veterinary and public healthservices.

Diagnosis. One of the major con-straints preventing control of zoonoticdisease outbreaks is the inability to di-agnose disease quickly and effectively.Most regional and district diagnostic lab-oratories are chronically under-equippedand under-funded, especially in the vet-erinary field. They are staffed by enthu-siastic, dedicated and trained people whoare a valuable, but under-used resource,and for whom there are few opportuni-ties for continued training and develop-ment. Targeting resources into theselaboratories would greatly enhance thediagnostic capability in the region.

Education. The final, and overwhelm-ing, need is for education at all levels. Itis imperative that health workers andveterinarians appreciate that both disci-plines contribute to the control of zoo-noses. Communication between dif-ferent ministries is essential to establishlinks at district and regional levels and aculture of collaboration should be de-veloped during formal training. This hasstarted very effectively in Ghana wherea Masters in Public Health course run bythe School of Public Health at the Uni-versity of Ghana trains veterinarians andhealth professionals simultaneously. Theexperience of the staff and students onthis course has shown that the inte-gration of medical and veterinary person-nel can work effectively. Finally, withouteducation and participation of local com-munities, any control effort is doomed.Small scale, local control campaigns in-volving the community and district healthmanagement teams are more likely tosucceed than large, cumbersome sys-tems imposed from above.

The workshop was opened by theHonourable Minister of Health forGhana, Samuel Donkor, who at the out-set instructed his Ministers to improvelinks between the Ministry of Health andthe Veterinary Services. Regional rep-resentatives present felt that there wasa similar political will within their owncountries to bring together health andveterinary professionals to improve thecontrol of zoonotic disease. The currentWHO focus on zoonoses, together withthe momentum and enthusiasm gen-erated at this meeting, should ensurethat some of these issues are actedupon. If targeted investment can be pro-vided, not just at the medical–veterinary

310 Parasitology Today, vol. 15, no. 8, 1999

News

interface, but at all those involved in thechain of food production, then there aregrounds for optimism for a more inte-grated solution to zoonoses in WestAfrica. This ‘plough-to-plate’ approachto public health is one which should beechoed around the world, not least inthe UK.

AcknowledgementsThe Workshop on Tropical Zoonoses inWest Africa was held at the NoguchiMemorial Institute for Medical Research in

Legon, Ghana, 3–5 February 1999. The suc-cess of this meeting was attributable to theenthusiasm and expertise of the regionalcontributors from Ghana, Nigeria, Togo,Burkina Faso, Tanzania and Zambia. We areparticularly grateful for the full support givento the meeting by the Honorary Minister ofHealth for Ghana, whose presence did muchto highlight the serious consideration thegovernment of Ghana has placed on thisissue. Financial and logistical support wasprovided by the British Council, Accra. Fullproceedings are soon to be published byActa Tropica.

Reference1 Gao, F. et al. (1999) Nature 397, 436–441

Jonathan Wastling is at the Division of Infec-tion and Immunity, Institute of Biomedical and LifeSciences, University of Glasgow, UK G12 8QQ.Dicky Akanmori is at the Immunology Unit,Noguchi Memorial Institute for Medical Re-search, University of Ghana, Legon, Ghana. DianaWilliams is at Veterinary Parasitology, LiverpoolSchool of Tropical Medicine, Pembroke Place,Liverpool, UK L3 5QA. Tel: 144 141 3304437, Fax: 144 141 330 4600, e-mail:j.wastling@bio.gla.ac.uk

One of the crucial questions in studies ofwildlife diseases has been whether para-sites typically influence host populationdynamics1,2. Several studies have demon-strated experimentally the detrimental ef-fects that parasites can have on fecundityand survival in wild animal populations(Table 1). Moreover, if parasites reducehost fecundity or survival in a density-dependent manner, it is quite possible thatthey might regulate host numbers3,4. Justdemonstrating these effects, however, isinsufficient evidence for regulation, as re-ductions in host fitness due to the pres-ence of parasites might act only in a com-pensatory fashion – that is, they mightaffect only individuals that would have low-ered fitness anyway as a result of otherregulatory forces, such as competition orpredation5. Host regulation by parasitescan be established only by experimentallyperturbing host/parasite systems awayfrom their equilibrium levels and monitor-ing subsequent changes in both parasiteand host densities relative to controls4.Such an approach has been applied suc-cessfully to captive systems (eg. an in-troduction of the nematode parasiteHeligmosomoides polygyrus to a breedingpopulation of laboratory mice reducedthe host equilibrium density by almost 20-fold6), but has proved difficult to apply tofield systems due to practical complexitiesand ethical considerations. Nevertheless,the first experimental proof that parasitescan regulate wildlife populations has nowbeen published by Hudson et al.7, whodemonstrate that parasitism by the gas-trointestinal (GI) nematode Trichostron-gylus tenuis is a significant factor in regu-lating populations of red grouse (Lagopuslagopus scoticus) in northern England.

The red grouse is a medium-sizedgame bird that inhabits the heathermoorland areas of Britain, where a largeproportion of its populations exhibit sta-tistically significant cyclic fluctuations inabundance, with cycle periods betweenfour and eight years8. Involvement of T. tenuis in these cyclic dynamics has longbeen suspected, because of the associ-ation between population crashes andhigh parasite intensities recorded fromindividuals. Traditionally, however, theactions of the parasite on the host were

not considered to be regulatory, rather,workers believed intraspecific compe-tition over food resources (principally theheather, Calluna vulgaris) to be the criti-cal driving force behind the cycles, withthe parasites acting only on weakenedindividuals in a compensatory manner to the intra-specific competition9. Thisview has now been proved incorrect.Using the experimental reduction of theparasite burdens in grouse at replicatedpopulations in northern England (bytreating individual grouse with an oral

News

Comment

Parasitology Today, vol. 15, no. 8, 1999 3110169-4758/99/$ – see front matter © 1999 Elsevier Science. All rights reserved. PII: S0169-4758(99)01484-2

Parasites Can Regulate Wildlife PopulationsD.M. Tompkins and M. Begon

Table 1. The impact of specific parasite taxa on the fecundity and survival of wild animals,as demonstrated through the experimental manipulation of parasite loadsa

Host Parasite Impact Ref.Anderson’s gerbil Synoternus cleopatrae Reduced survival 15(Gerbillus andersoni) (flea)

Barn swallow Ornithonyssus bursa Reduced fecundity 16(Hirundo rustica) (mite)

Cliff swallow Oeciacus vicarius Reduced fecundity 17(Hirundo pyrrhonota) (bug)

European starling Dermanyssus gallinae Reduced fecundity 18(Sturnus vulgaris) (mite)

Ornithonyssus sylvarium Reduced fecundity 19(mite)

Great tit Ceratophyllus gallinae Reduced fecundity 20(Parus major) (flea)

House martin Oeciacus hirundinis Reduced fecundity 21(Delichon urbica) (bug)

Pearly-eyed thrasher Philinus deceptivus Reduced fecundity 22(Margarops fuscatus) (fly)

Purple martin Dermanyssus prognephilus Reduced fecundity 23(Progne subis) (mite)

Red grouse Trichostrongylus tenuis Reduced fecundity 24(Lagopus lagopus) (nematode) Reduced survival 25

Snowshoe hare Obeliscoides cuniculi Reduced survival 26(Lepus americanus) (nematode)

Soay sheep Teladorsagia circumcincta Reduced survival 12(Ovis aries) (nematode)

a This is a complete list of studies known to the authors.