The role of field irrigation canals in the transmission of Schistosoma mansoni in the Gezira Scheme, Sudan

Bulletin of the World Health Organization, 59 (5): 777-786 (1981) The role of field irrigation canals in the transmission of Schistosoma mansoni in the Gezira Scheme, Sudan A. FENWICK,1 A. K. CHEESMOND,2 & M. A. AMIN3 This study was carried out to determine the importance ofsmallfield irrigation canals (abu eshreens)-of which there are over 22 000 in the Gezira Scheme- in the transmission of schistosomiasis. The observations were made during a 12-month period, November 1976-November 1977. The results indicated that during the 4-year crop rotation the abu eshreens supported snailpopulations in only two seasons, when they were irrigating crops of eithe, cotton or groundnuts. Thus, when agricultural labourers built temporary dwellings on the abu eshreen banks during these periods, the probability of finding infected snails was high. The maximum risk periods occurred during vegetable harvesting (including groundnuts) (October-December) and in the cotton picking season (January-April). Certain special situations lead to some abu eshreens playing an even greater and more predictable role in transmission. These occur when abu eshreens: (a) irrigate eucalyptus or fruit trees; (b) irrigate a block inspector's garden; or (c) are situated very close topermanent villages. Possible control measures to reduce the transmission potential of abu eshreens are discussed. These include improved maintenance and the use of either focally sprayed or slow- release molluscicides. The Gezira Irrigation Scheme was started in 1924 with the completion of the Sennar Dam on the Blue Nile, and with the addition of the Managil Extension, which was opened in 1963, it now compromises 800 000 hectares. The scheme is situated to the south of Khartoum, between the Blue Nile and the White Nile. The land is farmed by about 100 000 Arab tenants who live with their families and other nontenant Arabs in villages throughout the area. The permanent Arab population is estimated at 1.5 million of which perhaps 50% are infected with Schistosoma mansoni (1-3). The prevalence of S. haematobium varies from village to village. Outside of the Arab villages there is a scattered population of over 0.5 million people made up of Gezira Board employees, irrigation workers, labourers from west Sudan, and Nigerian immigrants. The first two categories are well housed by the I Principal Scientific Officer, Centre for Overseas Pest Research, Wrights Lane, London, on secondment to the Gezira Schistosomiasis Project, P.O. Box 2371, Khartoum, Sudan. Requests for reprints should be addressed to Dr A. Fenwick, at the Sudan address. 2 Lecturer, Department of Sociology, University of Hull, Hull, England. 3Leader, Gezira Schistosomiasis Project, Professor of Parasito- logy, Department of Community Medicine, University of Khartoum, Khartoum, Sudan. Government, but the Sudanese and Nigerians live either in temporary housing in the fields or in semi- permanent unregistered villages with no services. The rate of S. mansoni infection in the field workers and their families is over 50% (3). During the annual cotton picking season there is a further influx of over 0.5 million people who stay, camped in the fields, from January until May or June. These migrants come either as bachelor labour from the far west of Sudan, or in family, and sometimes village groups from outside the boundaries of the Scheme. Among the migrants who visit the Scheme on a regular basis, the infection rate is again in the region of 50/o (unpublished data, 1978). The Gezira irrigation network consists of a series of open, mud-lined, gravity fed canals distributing water in the following sequence: from the main canal, to the major canal, then to minor canals, and finally to field irrigation canals called abu eshreens. All these canals, but particularly the minor ones, form excellent habitats for the snails Biomphalaria pfeifferi and Bulinus truncatus, which are the intermediate hosts of Schistosoma mansoni and S. haematobium, respec- tively. In 1974 a routine snail control regimen was introduced, which consisted of 5 aerial sprays with the molluscicide trifenmorph over the main, major, and minor canals in the most northerly 80 000 hectares (4, 4115 -777- A. FENWICK ET AL. 5). The regimen was continued for 3 years and its effects were regularly monitored by surveilIlnce and sampling for snails, and parasitological examinations in preschool and school age children. The results suggested that the objective of keeping the minor canals virtually snail free had been achieved, but the incidence data gave equivocal results (6) since in some villages there was evidence that transmission was as high as in a nearby untreated area. It was these results that led us to carry out the present study to determine under what conditions the field canals (abu eshreens) might act as snail habitats and transmission sites. Since the aerial spray method of molluscicidal application cannot affect snails in those abu eshreens that are closed on the day of spraying, one possible reason for the continuing transmission in villages near minor canals that were regularly treated may have been the persistence of snails in some abu eshreens. The experimental area (Fig. 1) This study focused on Toba minor canal, which is 4.8 km in length, and is flanked by 17 fields on each side (south bank: A, -Q1; north bank: A2-Q2) (Fig. 1). Each field has its own abu eshreen that takes its water from the minor canal through a 30-cm diameter pipe, which can be sealed by a flange or mud plug when not required. The fields are divided into 4-hectare holdings by abu sitta canals that run the 300 m from the abu eshreen across the breadth of the field. Fig. 2 shows the crops on each of the fields at the time of the study and the position of any human dwellings, however temporary, that were built during the observation period. There were 2 permanent villages in fields A2 and B2 that housed agricultural labourers and their families. In T17 there were 114 people of Nigerian origin, and in T16 there were 60 people from the Fur tribe and 60 people from the Tama tribe-both from West Sudan. In field H2 there was a field inspector's house in a 2-hectare garden. The scattered dwellings were mostly temporary huts built either by migrant cotton pickers or by residents of T16 who preferred to camp near to the fields in which they were working. The camp labelled CP was erected in January 1977 by villagers from the east of the Blue Nile who stayed picking cotton and grazing stock until June 1977 when they returned home. The Arab tenant farmers whose holdings were in the study area lived either in Angado village (Fig. 1) or in another village 2 km to the east of Talbab major canal. Of the 34 abu eshreens, 4 were excluded from the study because they did not take water from the Toba minor canal. Fields C1, D1, and E1 were irrigated by water from Koa minor canal to the south, and field L2 was irrigated by water from Gad el Ain minor to the north. Of the 30"abu eshreens included in the study, all except A1, B1, and A2 followed the normal crop rotation of cotton-wheat-groundnuts/sorghum- fallow. Since the relatively low-lying land at the tail of the canal was prone to flooding, the Gezira Board allocated 2 fields to eucalyptus for fuel and building and left field A2 for fodder and casual cultivation by the T16 and T17 labourers. MATERIALS AND METHODS This study was carried out during the 12 month period from November 1976-November 1977, i.e. the latter half of one agricultural year and the first half of the next. -Once a week-except when heavy rainfall closed the roads during August and September-the area was inspected by driving slowly in a Land Rover alongside the Toba minor canal from its offtake to its tail, stopping to take notes at every abu eshreen, using a sketch map. The following observations were recorded: (a) Water levels, turbidity, flow rate, and vegetation in both the minor canal and in every abu eshreen. (b) Any human water-contact activities-such as, bathing, swimming, washing, drinking, fording, irrigating, fishing, and collecting water in tins. (c) Any human activities in the fields, for example, irrigating, planting, weeding, harvesting, house- building, shepherding, or defaecating. There was no identification of the individuals involved-but where possible, tribe, sex, and estimated age were noted. (d) The state of all the crops on each field. Snail sampling Forty potential snail sampling sites were selected from the map: the headwater pools of 30 abu eshreens, 7 abu eshreen sites opposite dwellings, and 3 abu eshreen sites near to dwellings. Some of these sites were dry and some never supported snail populations. Others supported snails for only part of the observation period. The aim was to examine each water-containing site at least once a month; sites of special interest were, in fact, visited more frequently. At each site visit, snail sampling was "exhaustive", that is, scooping was continued until the number of snails captured per scoop was much lower than at the start and usually took one man 30 minutes. For example, snail recoveries might drop from over 30 snails per scoop to 2 or 3 per scoop, or in a less densely populated site from 2 or 3 per scoop to zero. 778 TRANSMISSION OF SCHISTOSOMA MANSONI IN THE SUDAN a - Shcrnfnt Mninr rranal ANGADO VILLAGE 0 05km. N .inor Canal Abu eshreen / Abu sita EIVILi I I ~ ~~~IATIR RR wood 0Rn ,I2i ri woods oRd9I[ 9 a 9 R9 B2~~~~~~~1~ LI I - 'I C, Di _ ~~~E, F, /0 G. ,-5H, ",-A II c a u Ji L- -o N, 01 PI QI lb C2 D2 E2 F2 G? HF.I J4ouse H ~~H2 I2 J2 K2 L2 M2 N2 02 P2 gAQ LlQkt Q9 Talbab Major Canal Ca U0 L- o C E a ID Fig. 1. The study area and the Gezira irrigation system. L I 4 I- . 779 I 7 780 A. FENWICK ET AL. CP cotton pickers Key x dwellings * sites harbouring infected snails A, Eucalyptus A2 Fallow B, Eucalyptus i lB2Cotton [Ti16 Fallow C, Cotton C2 Fallow Do Cotton D2 G.nuts/sorghum E, Fallow E2 Cotton F, Wheat F2 Wheat G.G nuts/o m XXG,IG.uts/srghum xX G2 G.nuts/sorghum XXX Hi Fallow H2 Fallow I Wheat I2 Cotton Gnuts/ XXX T, sorghum &X JT2 Wheat Xxx _ _ _ _ _ _ _ _ _ _ _ _ _ _ K, Cotton K 2 Fallow L Cotton Toba L2 Cotton G. nuts! x MinorM G nuts/ XX X Minor M2 Gnuts/sorghum CPM, sorghum XX X X Canal x N Fallow N2 Fallow X ,_ _ _ __ _ _ _ __ _ _ __ _ _ _ 01 Cotton 02 Cotton X x x x Pi G.nuts/sorghum P2 G.nuts/sorghum Q Wheat 02 Wheat ff take Talbab Major Canal Fig. 2. Crops, dwellings, and infected snails within the experimental area. TRANSMISSION OF SCHISTOSOMA MANSONI IN THE SUDAN Collections were made in the evenings (16 h 00- 18 h 00) and early morning (05 h 00-07 h 00). The collected snails were then examined (between 07 h 00 and 11 h 00) for patent trematode infection in the field laboratory. This was done by separating the snails into species and screening all Biomphalaria and Bulinus in groups of 10, in clean water, in 74 mm x 25 mm glass tubes exposed to sunlight. Any tubes containing cercariae were quickly emptied and the snails were rinsed in clean water before being re- exposed individually to identify the infected specimen(s). The number of snails of each species in each collection, was recorded and the maximum shell width of the Biomphalaria pfeifferi was measured to the nearest millimetre. After examination, all snails were returned to the site from which they had been collected. No snails were crushed to determine the prevalence of immature trematode infections. On some occasions snails were carefully dried and then marked with nail varnish prior to returning them to their original site, in an attempt to estimate the stability of snail populations. RESULTS Abu eshreens as habitatsfor snails The abu eshreens can be classified according to the current crop being cultivated on the field they irrigate, which in turn determines the irrigation requirements for a 12-month period. Fig. 3 shows when an abu eshreen should contain water, and the months when they are expected to contain snails. Table 1 shows the actual drying out date in relation to the crops being cultivated, for the 30 abu eshreens under observation: Cotton. Only 2 of the 7 were dry by the end of April, 4 by end of May, and 2 (LM1 and OP2) did not dry out during the summer. Wheat. All six followed the expected pattern of November opening, and closure by the following April/May. Groundnuts/Sorghum. Only 1 out of 8 was dry by January, and 4 were allowed to remain wet into April. Fallow. Two of the 7 were never completely dry because AB2 acted as an overflow for Toba minor canal, while HI2 was open to irrigate the garden of the field inspector's house. Eucalyptus. Both abu eshreens were allowed to dry out in March so that the trees could receive their annual thinning. These results indicated that in addition to the months when snails might be expected to populate abu eshreens, inefficient water management could cause a delay in the drying out of abu eshreens and consequently in snai. deaths. Cotton abu eshreens should be dry by late March and groundnut abu eshreens should be dry by late December. If they are not, their snail populations will not be completely decimated. Table 1. Abu eshreens on Toba minor canal. Periods of dryness in relation to crop Cotton Wheat Groundnuts/dura Fallow Eucalyptus Field Abu When Field Abu When Field Abu When Field Abu When Field Abu When eshreen dry eshreen dry eshreen dry eshreen dryC eshreen dry B2 BC2 March F, FG, April D2 DE2 Jan. A2 AB2 Feb.a Al AB, March E2 EF2 April F2 FG2 May G, GH, Feb. C2 CD2 Dry B, BC, March 12 IJ2 May 1I IJ, April G2 GH2 Feb. H Hi, Dry K, KL1 May J2 JK2 May J, JK, April H2 HI2 Mayb L, LM1 Never Q, QO /M April M, MN, April K2 KL2 Dry dry 0, OP, June Q2 Q2/M May M2 MN2 April N NO1 Dry 02 OP2 Never P, PQ, April N2 NO2 Dry dry P, PQ2 March a AB2 acted as an overflow to Toba minor. b HI2 was wet only at the head. It irrigated the field inspector's garden. c Dry means that the abu eshreen was bone dry for the season. 781 A. FENWICK ET AL. C 4-- IA 00 0- Cl., -C 782 TRANSMISSION OF SCHISTOSOMA MANSONI IN THE SUDAN However, with efficient water management, the periods when snails would be found in abu eshreens would be limited to the months of October-March for cotton and eucalyptus, September-December for sorghum/groundnuts, and March-April for wheat. Abu eshreens as transmission sites Table 2 shows the results of the snail sampling and screening and indicates the relationship between the presence of infected snails and the presence of dwellings (see also Fig. 2). The 2 sites, BC1 and BC2, although not strictly adjacent to the dwellings in T16, were the nearest water-contact sites to Ti 6 in February and March when abu eshreen BC2 was dry. The transmission pattern in Gezira abu eshreens can be defined as follows: Cotton abu eshreens. By November Biomphalaria pfeifferi snails populated the cotton abu eshreens. Their numbers increased in proportion to the weed growth from December to March, but once the abu eshreen was closed the snail population was greatly reduced by dessication. Dwellings were built on the banks of some of these abu eshreens by sorghum harvesters (as with 0P1 ) in November, by groundnut harvesters (OP,, OP2) in December, or by cotton pickers (LM1) any time between January and May. In such cases there was considerable water contact, as the temporary residents used the abu eshreen water for drinking, cooking, laundry, and washing. After dwellings had been erected, infected snails were found in LM,, 0P1, and OP2. Infected snails were found also in BC2 near the permanent village T16. In those cases where no dwellings had been built on the banks of the abu eshreens, water contact-and hence potential contamination-was much reduced. However, there was always the possibility of infected faeces being deposited in or near an abu eshreen by a passer-by; but in fact no infected snails were found in any cotton abu eshreen without a nearby dwelling. Wheat abu eshreens. Since the wheat abu eshreens were opened only after dredging in October they remained weed and snail free until March/April and dried out soon afterwards. Therefore they are unlikely to have been important as transmission sites. Sorghum/groundnut abu eshreens. The presence of snails in these abu eshreens coincided with the November/December harvesting season. During these two months the abu eshreens supported aquatic weeds, emergent grasses, and many snails. These snails survived until the canal finally dried out but this process was delayed by the thick vegetation. Field workers built huts on the banks of the abu eshreens both to protect harvested crop and to be nearby for harvesting (JK1, GH1, MN2, PQ2). Again water contact by the residents of these huts was regular and the resulting contamination led to the presence of infected snails. Thus the potential for transmission existed in every sorghum abu eshreen Table 2. Patterns of snail sampling and infection rates in abu eshreens in the study area Snails infected 4 2 4 2 4 Month infected November November February March November June June November January 3 February March 5 November February March 3 March July 0 Total 22 486 Abu eshreen Total snails examined BC, BC2 (head) BC2 1T16) 5 640 713 128 GH, JK, LM, MN2 (huts) 189 219 522 1 247 MN2 (head) OP, OP2 17 Other sites Crop Eucalyptus Cotton Cotton Groundnuts Groundnuts Cotton Groundnuts Groundnuts Cotton Cotton 1 206 2 252 1 948 8 422 Nearby huts T16 T16 T16 Tama Tama Tama Tama Tama Tama (groundnuts) Tama Nil 783 29 A. FENWICK ET AL. from October until December or until it dried out. Fallow abu eshreens. Once the sorghum/groundnut abu eshreens were dry, they remained dry for 15 months before being redug and opened to pre-irrigate the cotton fields. Therefore they can be ignored as transmission sites except when they are opened in special situations such as for the field inspectors' gardens. Eucalyptus, citrus and special situations. There are three situations in which the 4-year cycle is not applicable and abu eshreens are opened on an annual basis from June to March-or remain open throughout the year: when the crop in the field is either eucalyptus or citrus; or when there is a block inspector's or field inspector's house, office, or garden, within the 36-hectare field. Snails may be found from October to March and sometimes all the year round. Infected snails may be found at any time of year. The abu eshreens are not usually near trees and these attract people because they provide both shade in which to rest and privacy, which makes them popular sites for defaecation, with subsequent washing in the abu eshreen. At the block and field inspectors' offices in Gezira, farmers are regular visitors on business and the abu eshreen banks provide shady meeting places. There- fore contact and contamination in these abu eshreens, with or without permanent residents, are greatly increased. The main activities are drinking, washing, ablution, and bathing. In October, as repopulation took place after the dry period, the sample collected from abu eshreen BC2 yielded 4 infected B pfeifferi out of 34. Fifteen days later 57 snails were collected from the same site but none were infected. Indeed only one of the previous 34 (which had been marked with nail varnish before release) was recollected in this later sample. Although water contact contamination took place in BC1 infection was detected only once. Thus, the more regular flow in these special abu eshreens may have a controlling effect on both miracidial penetration and the stability of the snail populations, although these abu eshreens are still potentially very important as transmission sites. Distribution of infected snails The overall picture illustrated by Fig. 2 and Table 2 shows that all 27 abu eshreen sites yielded snails in at least one visit and of these, 10 sites (Fig. 2) supported at least one infected snail. Of the 22 486 snails collec- ted over the year, only 29 (0.13%o) were found to be shedding S. mansoni cercariae, and they were all in sites near dwellings where water contact contami- nation had been observed. Of the 10 infected abu eshreen sites, 5 were irrigating cotton, 4 were irrigating groundnuts, and 1 was irrigating eucalyptus trees. Control of transmissiodn in abu eshreens From Fig. 4 it can be seen that the normal Gezira abu eshreen should contain water for only 24 months in every 4 years and is likely to harbour snails for only 13 of those months. Transmission is most likely from October to December when the crop is sorghum/ groundnuts and from October to April with cotton. When snails are present and dwellings are con- structed near to the abu eshreens, infection of snails will probably occur. The results also showed that incorrect water management may increase the period when transmission can take place. In the Gezira, some 6000 fields are planted annually with cotton, 6000 are planted with sorghum, groundnuts, and vegetable plots, and there are about 1000 extra abu eshreens near block inspector's, field inspector's premises, citrus gardens, or eucalyptus trees, i.e., about 13 000 potential transmission sites. Of 30 abu eshreens fed by the Toba minor canal, 29 infected snails were recovered from 10 sites. This is not a high rate of infection compared with recoveries from the water-contact sites in minor canals (e.g., 50 infected B. pfeifferi were found in one Toba minor site in December out of 1259 collected) but as limited foci with a high transmission potential they should be included in any control planning. The following action could be taken to minimize abu eshreen transmission: (a) Improved water management. As soon as the abu eshreen has completed its function for the season it should be closed and drained immediately. This requires the cooperation of the field inspectors, water guards, and farmers, and proper delegation of responsibility. The water guard should be instructed to see that the outlet pipe is well sealed and the canal drained to speed up the natural drying process in December (for groundnuts) and April (for cotton). (b) Redigging. Scouring the dry abu eshreens in February for cotton crops and in October for wheat crops removes weeds and appears to delay snail re- population. If the wet abu eshreens could be cleaned by machine at intervals during the high risk periods some degree of snail control should result. (c) Focal mollusciding. Efficient treatment with focal molluscides requires an enormous number of applications at a large number of sites. A possible alternative control measure would be the suspension of a slow release formulation of a molluscide inside every abu eshreen pipe. This possibility will be tested in the Gezira in the near future. 784 TRANSMISSION OF SCHISTOSOMA MANSONI IN THE SUDAN ~ ~ ~ ~ ~ ~~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~ C3 CL 0f 0 CC C,) 0 CU 0 ri .4-* 0~~~~~~~~~~~~~~ o) v- 0~~~~~~~~~~~ 785 786 A. FENWICK ET AL. ACKNOWLEDGEMENTS We wish to thank the Edna McConnell Clark Foundation (Grant N° 278-0014), the Medical Research Council of the Sudan, and the Overseas Development Administration, United Kingdom of Great Britain and Northern Ireland, for their financial support. We also thank Dr A. Davis and Dr W. Sands for their encouragement and advice during the study, and for reviewing the manuscript. RESUMt ROLE DES CANAUX D'IRRIGATION DANS LA TRANSMISSION DE SCHISTOSOMA MANSONI DANS LA ZONE DU PROJET DE GEZIREH, SOUDAN Dans la zone irrigu& de Gezireh, au Soudan, vit une popu- lation arabe autochtone d'environ 1,5 million de personnes, auxquelles il faut ajouter 0,5 million de non autochtones composes essentiellement d'ouvriers agricoles, plus un apport saisonnier de plus de 0,5 million de cueilleurs de coton. Le taux d'infection general par Schistosoma mansoni depasse 50%o, et les efforts de lutte contre la schistosomiase au moyen d'applications generalisees de molluscicides n'ont pas donne jusqu'ici de resultats satisfaisants. La poursuite de la transmission de l'infection dans les villages o'u les canaux mineurs proches sont regulierement traites s'explique peut-etre par la presence de populations de mollusques dans les canaux des champs (abu eshreens). On a donc entrepris une etude des abu eshreens pour determiner la mesure dans laquelle ils jouent un role dans la transmission. On a observe les contacts de la population avec l'eau dans une zone experimentale englobant un canal mineur et 34 abu eshreens et parallelement on a procede a l'examen d'echan- tillons de mollusques et au depistage des cas d'infection manifestes. Il ressort de l'etude que les abu eshreens contiennent en effet des mollusques, mais qu'au cours de leur cycle qua- driennal d'irrigation regi par la rotation des cultures, il n'y a que deux grandes periodes de transmission possibles: lorsque les abu eshreens sont utilises pour l'irrigation des arachides et des legumes, de septembre a janvier, puis lorsqu'ils sont utilises pour l'irrigation du coton, d'octobre A avril. Les chances de trouver des mollusques infectes dans les abu eshreens au cours de ces deux periodes augmentent conside- rablement lorsque les ouvriers agricoles ou les cueilleurs de coton se construisent des logements provisoires dans les champs au bord meme des abu eshreens. On pense que I'application focale de molluscicides, c'est-A-dire l'introduc- tion reguliere de petites quantites de niclosamine dans les abu eshreens, le premier jour de chaque mois par exemple pendant la saison de transmission, serait une mesure de lutte pratique que pourrait appliquer les travailleurs eux-memes conformement au principe d'auto-assistance. Une gestion plus stricte des eaux, en particulier en ce qui concerne la fermeture des canaux, une fois termine leur fonc- tion d'irrigation pour la saison, contribuerait egalement a la lutte contre l'infection. Pour certains abu eshreens (jusqu'a 1000), le cycle qua- driennal d'irrigation n'est pas respecte pour des raisons sp6- ciales. Dans certains cas, en effet, les abu eshreens restent ouverts presque en permanence pour irriguer les plantations d'eucalyptus ou pour fournir de l'eau pour les bureaux ou les jardins des inspecteurs de bloc et des inspecteurs de terrain. Dans ces abu eshreens, on a pu trouver des mollusques en permanence et le contact accru avec l'eau qu'entraine l'exis- tence de jardins et d'arbres a provoque une augmentation de la transmission. L'application focale reguliere de mollus- cicides par les occupants des bureaux est suggeree a titre de mesure de lutte. L'etude a montr6 que les 22 000 petits canaux d'irrigation des champs dans la zone de Gezireh jouent un role important dans la transmission, mais elle indique que les periodes de transmission sont previsibles, de sorte que des mesures de lutte pourraient etre mises en oeuvre par la population elle- m8me, une fois celle-ci dfiment informee des aspects sani- taires de la question. REFERENCES 1. AMIN, M. A. 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