Control of schistosomiasis — A global picture

Reviews

Control of Schistosomiasis- A Global Picture L. Savioli, E. Renganathan, A. IHontreso~, A. Davis and K. Behbehani The control of schistosomiasi, s h,Ts been a clufflcnging task for most endemic countrie.~. Thus, despite the concerted efforts to date, schistosomiasia remahts a major public ht~lth concen~, ~'cond onh,I to malaria in the tropics trod subtropics, in this review, Lorenzo Savioli m~d colleagues highlight cha~ges in schistosomiasis pr~,alence attd distribution over the past decades, discuss the success and limitations of the various conh'ol strategies, and present possible control initiatives [or the future. In 1947, Stall, in a famous address to the American Society of Parasitology ~, estimated that 114 million people were infected with the three schistosome species pathogenic to humans: Schistosom,~ japonicum, S. hacmatobium and S. mansonl. Schistosoma japonicum was estimated to be the most prevalent, with 46 million people infected with this species in six countries including Japan:, while $ haematobhon and S. mansom were estimated to account for 39 million and 29 million infections, respectively. Obviously, S. mekongi did not feature in StoWs presen~a,~on, as it had not yet been described 3. Although an S. japomcum-l~ke irdection was first described in a patient in Thailand in 1950, the p~'obable cau~tive agent, S. mekongi, was not identified as a new species until 1978 (Ref. 4). Stall included S. intercalatum with S. haematobium in his estimatesL The global d~stribution of the disease has changed sig~,ificantly in the past 50 years, with control successes achieved in Asia, the Americas, North Africa and the Middle East. However, despite this progress the disease remains endemic in 74 developing countries and inf~ts more tha~ 200 r~illion people s (as compared with the 1!4 million/:maple estimated to be harbouring the infection 50 y e a ~ agog). Of these, 20 million suffer severe consequences firom the disease and 120 million are symptemafics. WHO estimates that, worldwide, 500--600 million people are ~till at risk of infections.

decrease [3.6% in 1994 (WHO, unpublished)] and transmission has ceased in some areas. The notable successes in Indonesia and the Philippines are due to intensive control efforts that should be maintained in the Iuture ~'. In China, an epidemiological survey in 1049 revealed that at least 12 million people were infected 7, in 1989, despite a significant increase in the population, this figure had dropped to 1.52 million 8. The relrnaining endemic ioc~.are now found in the swampy and lake regions of southern China, which cover a vast area of five provinces (liangsu, Anhui, Hubei, ]iangxi and Hunah)L Despite the progress in the COlatrt,l' of schistosomiasis in China, the diseaso is still a significant public health issue and there are increased risks of transmission as a result of several ongoing water resources development schemes, in particular the Gorges Super Dam Project on the Yangtze river. These develop'.rmnts require the adjustment of present control activities to the new challenges and there is a need to strengthen current control strategies.

Schistosoma haemetobium The prevalence of S. haematobium has dropped significantly i~ several countries of North Africa and the Middle East, while transmission has ceased in Tunisia, Oman and Lebanon. Specific targets for eradication have also been established in Algeria and Morocco~. Nevertheless, urinary schistosomiasis continuc,s to be of public health concern in vast areas of Africa and the Middle East. In Zimbabwe, for example, although there is a long history of commitment towards morbidity contrel through the primary health care system, haematuria remains among the top ten reasons for attendance at health facilities9. In Yemen, concerted control efforts have only recen_t!y been started with the support of WHO ".

Schistosoma mansoni Schistosomiasis control in the Caribbean has been a success story. There has been a very marked reduction of transmission of S. mal~soni in Guadeloupe, Martinique and St Lucia, and Antigua has not reported any cases for many years 6. In the Caribbean, probably only Puerto Rico and the Dominican Republic have active areas of transmission, with 70000 people at risk ~. In Africa, major man-made en ¢ironmental changes in ESypt, Mauritania, Senegal and Ghana have ~een associated with an increase in schistosomiasis transmissior,. In many of these areas, there has been a The authors are at the VVofld Health Organization. 121 I Geneva 27. selective increase of the transmission of S. man~o~i. Switzerland: L~rmnzo Sa~-toli and Antonio blor~tresor are The increase in both prevalence ai.d distribution of S. at zhe Division of Control of Tropical Diseases.Schistosomiasis mansoni has been associated with a concurrent reducand Intes'inat ParasitesUrit: Eiii Renga:~athanis at the Division of tion in S. haema~obium infection~ ii bas been sugCc,ntrol ¢,cTropical Diseases.Training Unit: Andrew Davis was forgested that increased salinity and the change ~rom rnedy the O~rector.Parasitic DiseasesProgramme; and Kazem seasona~ flooding to perennial irrigation after ihe Beabehani is Director of the Division of Control of Tropical Di-~eases.Teh +41 22 7912664, Fax: +41 2Z , ~ 141~9, completion of the Aswan High Dam led to the pree-mail: ~olg~WHO.~H dominance of Biomphalaria species over Bulimls in the

$chistosoma japonicum Schistosoma japonicum, the predominant of the three major schistosome species in StoWs estimates and the most difficult to control because of its zoonotic nature, lkas now been effectively controlled in many areas. It is presently endemic in only three countries - China, Indonesia and the Philippines - and rontrol efforts have significantly reduced transmission. In the rare fo~ remaining in Indont~ia, prevalence is now less than 1%. In the Philippines, prevalerlce continues to

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PcIrCJSi[OiO~'~ Today, vol 13, no. r I, 1 9 9 7

Reviews Nile Delta t°. In the irrigated areas of the Nile Delta !°, intestinal schistosomiasis is now more common than u r i n a ~ schistosomiasis. The first transmission of S. mansoni in Mauritania was reported in 1996 - after completion of the Diama Dam on the Senegal river in early 1988 (ReL 11). The first eases of S. man,qoni infec.l.lon were reported in Senegal one and a half years after the dam became operational, and in the last quarter of 1989, 71.5% ol 2086 routine stool examinations were positivr, for schistosomiasis in the village of Rl,rhard TolP 2.

Country profiles: Egypt and Brazil as ~.xampies Two major programmes currently dominate schistosomiasis control and research in Egypt: the Ministry of Health's Schistosomiasis Control Programme, which has been engaged in a concentrated nationwide control campaign since the early 1970s; and the Schistosomiasis Research Project operating since 1987 (Ref. 13). Successful control efforts have led to a dramatic drop in prevalence of infection from 30% to 6% in Upper Egypt, an area largely endemic for .q..haematobium. In contrast, although knowledge of schistosomiasis has been improved, attitudes and practices have still not changed substantially in many rural areas 13. S. mansoni is also more difficult to control and the prevalence remains around 15% in the middle and eastern Delta regions. Thus, schistosomiasis remains a major public health problem in Egypt. The significant reduction in prevalence rates in the vast five decades is not obvious in numerical terms d u e to the fourfold increase in the population over this time; thus, the estimated number of infected people is still close to the six million indicated by Stoll in 1947 (Refs 1, 5). !~ this situation, maintenance of conh'ol and monitoring is clearly needed to prevent a further rise in prevalence following reinfection after chemotherapy. In Brazil, in contrast, there has been an obvious reduction in the schistosomiasis-related severe morbidity commonly seen during the 1950s. In addition, there has been a significant reduction in morta!ity due to S. mansoni during the past 20 years. From 1977. to 1988, for example, the mortality fell from 0.67 to 0.47 per I.,00000 inhabitants, corresponding to a reduction of 34% (Ref. 5). Now a major challenge in Brazil is that of co-ordinating efforts with ministries and institutions responsible for education, water supply and sanitation, in order to address the problem in endemic areas 5. The strategy for successful schistosomiasis control While no patent recipes are available for application in all instances, experience in countries where mortality, morbidity and transmission due to schistosomiasis have been effec~vely controlled shows that the strategy endorsed by the WHO E×pert (-ummittees in 1984 and 19'91 (Refs 2, 5) is a feasible and effective one (Box 1). In ereas of high endemicity, population-based chemotherapy has beon able to reduce dramatically the prevalence and -3everity of the morbidity associated with the infection. In addition, the recommended provision .~f safe and adequate water supplies and sanitation contribute~ substantially to reducing the prevalence and severity of schistosomiasis14. Purasitology Today, vol, 13, no, I I, 1997

The role of molluscicides in schi,~tosomiasis control progran~mes depends very much on local epidemiological and ecological circumstances, coupled with the human and financial resources available. However, within the context of a larger concerted intervention, focal mollusciciding of major transmission sites in high-endemicity communities is a feasible approach. Snail control has not always produced the desired effects and the eradication of the intermediate host has been possible only in a few extreme situations soch as in oases in Tunisia. Environmental modifications to eliminate the intermediate host are possible and, on a large scale, have been highly effective m parts of China s. In general, it has e.nly been through the integration of complementary strategies, such as chemotherapy, health education, water supply and sanitation, that effective disease control has been achieved in many countries outside Africa. Impact of water resources development on schistosomiasis transmission Within the general development process taking place in Africa, particular emphasis is being given to water resources management. Increasingly, dams and irrigation systems have become indicators and symbols of development. Public attention is focused mainly on the large *~,ater development projects of the tropical world because of their intrinsic scientific engineering interest and ",heir symbolic value for haman achievement. In Ghana, the construction of a dam on the river Volta in 1964 created the world's largest man-made lake. As a consequence, the prevalence of c. haematobium infection, which was 5-10% in the Voile basin before construction, increased to about 90% in the same area in 1969. However, it is likely that the construction of smaller, less publicized, village dams may have even greater significance for human health. Small and accessible water supplies tend to s e r v e more p u ~ than do larger dams. They may be used for fishing, water supply and irrigation, and this ~,pe of water source has a high degree of contact with people and animals, increasLng the potential for intensifying or spreading schistosomiasis and other water-borne and vector-borne diseases9. The rate at which these dams arc built, and the lack of environmental and health considerations in the planning phase, often lead to a situation where the capacih, of the health care system to deal with the cordequences of these developments is grossly inadequate. Much cited examples include Cameroon, where the construction of over 1O0 small artificial lakes for fish culture led to a considerable increase in schistosomiasis and other water-associated parasitic infections 15, and Ghana, where the prevalence of 5. haematvbium ~ript,.~,.! after the construction (between 1958 and 1960) of 104 small dams in the north-east of the country ~. New challengers ahead In many countries, the successes ot the control programmes are also associated with new challenges for the future. One such prt~blem is linked to rapid urbanization taking place in the developing world. In the north-east of Brazil, prevalence appears to be 445

Reviews _

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programmes in Ghana, Zimbabwe, Tanzania 17 and other countries, have shown the feasibility of using haematuria to identify schoolchildren requiring treatment for S. haematobium infection in a highly endemic The strategy (outlined in Ref. 5) covers a range of joillt mea (Fig. I). Subsequent treatment of those testing initiatives, including: positive has led to a rapid decrease of clinical Provision of diagnosis and treatment at the primary morbidity due to S. haematobimn, without tb.e need health care level for laboratory facilities and at relatively low cost. • Selective or mass chemotherapy Experience has also shown that in highly endemic • Health education • Control of intermedi;~te ilosts areas the prevalence and intensity of urinary schisto• 9upply of drin~ ing water and planning of adequate somi,~sis among schc,ol-age children are practical epihealth care facilities demiological indicators of the status of its transmis• Environmental mal:agement sion in a community. In Zanzibar, Tanzania, areas to be t;~rgeted for complementary intervention have been accurately defined by post-treatment examinrising where the disease has been introduced in pertation of schoolchildren, who are at the highest risk of urban areas through rural-urban migration and the re-infection17. availability of new breeding sites for the snail host. Another important a~d:~k~ to community-based Refugee movements, as a consequence of war and control tools has been the use of rapid assessment natural disasters, are also contribuling to the spread questionnaires. These simple questionnaires, initially of the d i ~ a s e to many previously schistosomiasisfree areas, such as in parts of Somali~. and Cambod~.a. developed and tested for urinary schistosomiasis, However, within the global epidemiolog:eal have been shown to be effective in identifying highrisk communities needing priority intervention. The picture, the major area of challenge for combating questionnaire can be easily addressed to schoolschistosomiasis remains sub-Saharan Africa. Effective children, who respond to simple questions such as tools for control are available and these must be those related to observed haematuria and history of implemeniccJ a vi,ropriztely. There is an urgent need schistosomiasis. It has been suggested that this for a renewed commitment by endemic countries and approach could substantially bring d o w n the cost of donors to control schisto~miasis it, ~.frica. Selective screening for infection18. Based on these initial findings, chemotherapy of individuals identified by ~eagent strips for haematuria, an indirect diagnostic sign, is a guide for use in cont~'ol programmes has been a simple and feasible approach for reducing S. haemadeveloped and is currently being tested in a number of African countries, while studi~s are under way tobium-related mod.*iditv at the peripheral health to test rapid assessment protocols for intestinal care level or in schooicfliIdretdL L~.rge-scale control schistosomiasis19. Currently, diagnosis followed by appropriate chemotherapy remains the cornerstone of our control strategy. At the moment, three effective and safe drugs are available for treating schistosomiasis: oxamniquine, metrifonate and praziquantel. For a number of ~easons, including commercial viability, oxamniquine and metrifonate may soon cease to be readily available, leaving praziquantel as the sole gene',',~!ly available drug. Praziquantel is the drug of choice for ca~e-management in schistosomiasis, and it is also the main tool of country-levd schistosomiasis control programmes. It has thus been administered to tens of milllon infected individuals in endemic countries. Toe progressive reduction in costs over the past ten years has ~Iso made the drug more readily available. This scenario, however, has recently been tainted by rel~}rt:~ of low cure rates in Senegal and the isolation of potential praziquantel-resistant schistosomes in the laboratory 2°,2t. These reporls need further confirmation. . . . . . . . . . . . . . . . . ~-i. . . . . . . . . . . . . . . . . . . . . . . . . i ........... •.................... In the meantime, there is a need c~rtae of S, haen~d)/urn in the water, and are th:.~ most dangerous for transmission. for ~ncreased vigilance in both Box 1. The Sirategy for"Schistosomiasis Control

Endorsed by the ~'tiG

Paro~rology Today, vol. 13, no. I l, 1997

Reviews Tab!e I. Treatment schedule for the ir~teg~'ated control of Schistesoma haematobiurn, intestinal nematodes and lymphatic filarias~,: in Zanzibar. United Republic of Tanzania

Schistosomiasis

Intestinal parasitic infections

Filartasis

Drug

Prazlquantel (40 mg kg ~ single do~e)

Hebendazole (500 rng single dose) or Albenclazole (400 mg single dose)

Iverraectin (200 Is.gkg ~ single dose) plus klbendazole

Target group

Schoolchildren I × yearly:

Schoolchildren 3× yearly:

Targeted mass treatment for the whole

Targeted mass trea£ment

C o m m u n i t y members ol(ller than two years I × yearly: Universal treatment

(400 mg single dose)

school in areas with prevalence of microhaematuria >20% Selective treatmer~: of schoolchlldren in areas with prevalence of microhaemamria <20%

Pre-sciiool children 2 >c yearly~ Tcrgeted ro.~ss treatmentin Koran schools Treatment at the MCH clinicsa when receiving vaccination Pregnant women I × during 0regnal~cy after first trimester Tr:atment at the HCH clinics when receiving ~accination

aMCH, mother and child he.-.!th.

monitoring and reporting of any emerging praziquantel t o l e r a n c e / r e s i s t a n c e , which would obviously have major implications for control strategies in the future. There is also a strong need to promote research and development of addilional ~mfi-schistosomal drugs. Immunological intervention in the form of a schistosome vaccine wo~ici complement the success of our present control efforts by adding to existing control strategies. Realistically, however, there is still some way to go before an effective vaccine will be ready for use within n-~tional contrt,! programmes. In additio:~, logistic d~ff~cL~lti~ssuch as d,:livery problems encounle¢~.d v~iL!,uL.'.:¢~already available vaccil',es may need to be considered before imp;cmentation. I n t e g r a t i o n w i t h o t h e r d i s e a s e - c o n t r o l activitie~ Integration of schistosomiasis control into the existing health structures has been consiAered essential in the maintenance phase of con~ol ?-~. However, most pritnary health care systems in Africa face a multitude of problems, while manpower, exF,~:',ise and resources are scarce. Present approach~,s, to us~ 'integrated disease control' are therefore insufficient. In many countries where schistosomiasis occurs, children are often concurrently infected with soilt,..ansmitte::l helminths. Schoolchildren harbour the most intense infections~ with adverse effects on health, growth and sc:~ool performance23. Both schistosomes and soil-transm!tted helminths can be treated with single doses of orally administered drugs: praziquantel is highly! effective against all three species of schistosome:, while benzimidazo!e derivatives such as mebendazole or albendazole are effective against soil-transmit::-~ helminths. The cost of delivering treatment, whether provided on the basis of mass treatment or of selective treatment to those infected, may be reduced considerably and compliance increased when both drugs are administered at the same time. Clinical trials supported by WHO on the abso:-l~:.ion, pharmacokinetics and safety of praziquantel and albendazo!e, when jointly administered, have shown that the combination is ~afe and Pa,'asitology iortoy, vol. 13. no. I I, •997

effective ('Health of school age children: treatment of intestinal helminths and schistosomiasis', unpublished WHO documei',;3. Schoolchildren arc also one of the most accessiole groups for treatment, and health care can be efficiently integrated with education programmes ('Report of the meeting between the WHO and the Partnership for Child Development'. unpublished WHO document). The Partnership for Child Development is carefully monP.oring school-ba~cd health and nutrition pl~ogrammes in Ghana, Tanzania, India and Indonesia. These programmes have :~hown that the education sector is capable of delivering a simple !:ealth package (health education, anthelmintics and sometimes also micronutrients) to large numbers of schoolchildren (50000 to 3 million) without the creoti~,-~ of SF~'cific infrastructure. Furthermore, they have shown that teachers perceive this role in health as an acceptable, even welcome, extension of their overall role in the community, and that both s ~ d e n t s and parents concur -with this view 24. These experiences together with those in other countries, like those in Tax:zafiia ('Report of the WHO Informal Consultation on tae r~se of chemotherapy for the control of morbidity ,'tt~*" to soil-transmitted nematodes in humans', Wl-'iO document) and the Seychelles~-;, suggest that the school system can contribute to health delivery, provided that the package is simple, demands little school time, and is perceived as appropriate to local needs. The tools and stra~.egies recex~tly developed 1or filariasis control are sinfilar to those used in controlli:',g morbidi,'y d - e to mtestmai nematodes and schistosomiasis ('Report of the WHO Informal C ~ sultation on the use of chemotherapy for the control of morbidity d~e to soil-transmitted nematodes in humans', WHO document). The most effective treatment for lymphatic filariasis is the use of two-drug regimens. Tabl,,• 1 shows a possible approach for the use of available tools for schistosomiasis, intestinal parasites and filariasis co~trol, which will ~ , applied in 1998 in Zanzibar. Better c~ordination and the combining of resources would: appreciably enhance the 447

Reviews h e a l t h i m p a c t of c o n t r o l efforts a g a i n s t these ( a n d p e r h a p s other) tropical diseases. S u c h c o - o r d i n a t e d e f f o r ~ a r e a p p e a l i n g to h e a l t h ministries a n d financial d o n o r s b e c a u s e t h e y a r e b o t h cost- a n d labot~r-effecfi:'e. Conclusions In t h e p a s t 50 y e a r s t h e g l o b a l p i c t u r e of s c h i s t o s o m i a s i s h a s changed, c o m ; i d e r a b l y . 5. japonicttm a n d 5. haematobium, the m a i n c a u s e s of infection in 1947, h a v e d e c r e a s e d in p r e v a l e n c e , i n t e n s i t y a n d d i s t r i b u tion, w h i l e S. mansoni h a s b e c o m e t h e m o s t p r e v a l e n t a n d w i d e s p r e e d of t h e t h r e e species. S u c c e s s f u l c o n trol o f s c h i s t o s o m i a s i s h a s b e e n a c h i e v e d in a n u m b e r of c o u n t r i e s a n d for all t h r e e m a j o r species. S u c h s u c cess h a s b e e n c o n s i s t e n t l y l i n k e d to b o t h political c o m m i t m e n t atld t h e i m p l e m e n t ~ f i o ~ of a concei'ted control strategy. However, recent environmental c h a n g e s closely l i n k e d to w a t e r r e s o u r c e s d e v e l o p m e n t , a n d i n c r e a s e s in p o p u l a t i o n d e n s i t i e s , h a v e led to t h e sp=¢ad o f t h e d i s e a s e to p r e v i o u s l y l o w o r no.aendemic areas. Water resources development projects t h u s n e e d to a d d r e s s h e a l t h i m p l i c a t i o n s m o r e closely, in p a r t i c u l a r the s p r e a d of w a t e r - t r a n s m i s s i b l e diseases. T h e greate~t c u r r e n t c o n c e r n is in A f r i c a w h e r e m o s t o f t h e t r a n s m i s s i o n is t a k i n g p l a c e d e s p i t e t h e a v a i l a b i l i t y of effective tools f o r d i s e a s e control. T h e r e is a n u r g e n t n e e d f o r a r e n e w e d c o m m i t m e n t b y e n d e m i c c o u n t r i e s a n d d o n o r s to c o n t r o ~, s c h i s t o s o m i a s i s in Africa, w h e r e it r e m a i n s seco,.~d o n l y to m a l a r i a in t e r m s of s o c i o - e c o n o m i c a n d p u b l i c health importance.

Acknowledgements This article is dedicatedto the memory of the late Kenneth Eugene MotL who. ove~the pa~tdecades,has devoted his Lifeto promoting the control of schistosomiasisand food-bo,mc trematodes. ~¢e acknowledgearid thank MarcoAlbonico for his contribution.We are also grateful to Don 8undy and David Crompton for their critical review of the manuscnptand their encou!~gement. Re~erenc~ 1 Stall, N.R. (1947) This wormy world. I. Parasitol. 33,1-18 2 WHO (1985) The Control of Schistosomiasis. Report of a WHO Expert Cmnmittee (T~hnical Report Series/"28), WHO 3 Beaver, P.C. et aL (1984) in Clinical Parasitoloet/(Beaver, P.C., Jung, R.C. and Cupp, E.W., eds), pp 415--448,Lea & Febiger 4 Voge, N. et al, (1978) Schistosoma mekongi sp. n. from man and animals, compared with fou¢ geographic strains of

M o r e on W o r m s : C o m i n g

$chistosoma japonicum. I. Parasitol. 64, 577-584 5 WHO (1993) The Control of Schistosomiasis. Second Report of the IArHO E.~7~ertCommittee (Technical ReDort Series S30), WHO 6 WHO (1997) Division of Control of Tropical Diseases. Pro,~ress Report 1996, WHO 7 Ross, A.G.P. et al. (1997) Schistosomiasis control in the People's Republic of China. Parasitol. Today 13, t 52-155 8 Zhen, J. (1993) A brief introduction to nation-wide sampling su~m,ey on schistosomiasis in China. Chin. Med. J. 106, 569-575 9 WHO (1993) in Parasitic Diseases in Water Resources Da~elopmeat. The Need for htterscctorial Negotiation (Hunter, J.M. et al., eds), WHO 10 Abdel-Wahab, M.F. el al. (1979) Changing patterns of schistosomiasis in Esypt, 1935--1979.~';;;cct2. 242-244 11 Urbani, C. et at. (1997) Parasiloses int.~stinales et schistosomiases dans la valise du fleuve S~n~gal, Repubtique Islamique de Mauritanie, Med. Trop. 57,157-160 12 Talla, A. (1990) Outhreak of intestinal schistosomiasis in the Senegal River Basin. Ann. 5oc. Brig. Med. Trop. 70,173-180 13 Davis, A. (1997) Recent advances in schistosomiasis in Egypt. Bull. Trop. Med. Int. Health 5, 5--6 14 Esrey, S.A. (1991) Effects of improved water supply and sanitation on ascariasis, diarrhoea, dracunculiasis, hookworm infection, schistosomiasis and trachoma. Bull WHO 69, 609--621 15 Ripert, C. and Raccurt, C.P. (1987) The impact of small dams in parasitic diseases in Cameroon. Parasitol. Today 3, 287-289 16 Savioli, L. and Mott, K.E. (1989) Urinary schistosomiasis on Pemba Island: low cost diagnosis for control in a primary health care setting. Parasitol. Today 5, 333-337 17 Savioli, L. et at. (1989) Control of morbidity due to S. haematobium on Pemba Island: selective population chemotherapy of school children te identify high ~sk localities. Trans. R. Soc. Trot~. IVied. ttyg ~71~~nr~.~110 Ig Lengler, C. et al. (1991) Rapid low-cost, two-step method to screen for urinary schistosomiasis at the district leveI: the [4.ilosaexperience. Bull WHO 69,179-189 19 WHO/TDR (1997) Tro:.,i,:,~ .Oisea~e Research - Thirteenth Programme Report, WHO 20 Stelma, F. et aL (1995) Efficacy and side effects of praziquantel in an epidemic fc.cv~ of Schistosoma mansoni. Am. J. Trop. Med. Hyg. 53,167-170 21 Fallon, P. et aL (1995) Diminished susceptibility to praziquantel in a Senegal isolate of Schistosoma mansoni. Am. ]. Trop. Med. Hyg. 53, 61-67 22 Korte, R. and Mott, K.E. (1989) Maintenance of schistosomiasis control: an overview. Trap. Med. Parasitol. 40,130-133 23 Savioli, L. et at. (1992) Intestinal parasitic infections: a soluble public heal~ problem. Trans. R. Soc. Tr~p. Med Hyg. 86, 353-354 24 Partnership for Child DeveloF,ment (19~7) Better health, nutrition and education for the sb ~*ol-agedchild. Trans. R. Soc. Trop. Med. Hyg. 91,1-2 25 Albonico, M. et aL (1996) Coniro~ of intestinal parasitic infections in the Seychelles: a comprehensive and sustainable approach. Bull. WHO 74, 577-585

S o o n in P a r a s / t o l o g y T o d a y

• G I o ~ ~ p i n g of lympha~c filari~sis, by E. Michael and D. Bundy • Schistosomiasis vaccines: ~he long and vdndl~ road, by I~ Berl~luist and D. Colley • Parasitic worms: an ally in the war on resistant microbes, byJ. Webster - Mu~-Ji.~g,'~.~n par~iric flatworms, by G. IVlair, .~G. Maule, C. Shaw and D.W. Haiton • Hookworm-provoked I~E-mecliated pathoio~: ~ s d ~ n ~ or remarkable strategy, by J. Croese • .¢x:h/stos~mtaja~bon/cum~ r biology and vacdng ~ t , by W.U. Tiu • Determinants of life hJstory e v ~ o n in n ~ , by $ ~ and G. Sorci • Vaccination again~ scht~osomiam: the case for lung-stage antigens, by A.P. Mounfford and R Harrop • Puberty, immunity and ,~[e-rel=r=l ~ in susceptibility to s~i~-tosome infection, by A.J.C. Fulford, M. Webster, J.H. Ouma, K. Gadmhi and D.W; Dunne Don't mira these, snd many o t ~ w ~ of interes~ mb~ribe to parmlto/or/Todw/ . the ~ p - d t e d Parut~losy ~aumal - ruing the form bound in this issue 448

Paras:tology Today, vol. 13, no. I I, 1997