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Cost-effectiveness of different ways of controlling intestinal schistosomiasis: A case study
COST-EFFECTIVENESS OF DIFFERENT WAYS OF CONTROLLING INTESTINAL SCHISTOSOMIASIS: A CASE STUDY* A. M. Laborator!
for Parasitology,
State University
POLDERMAN
of Leiden. Wassenaarweweg
62, Leiden. The Netherlands
Abstract-Intestinal schistosomiasis is highly prevalent among the labourers and their families in many of the miners’ villages in Maniema, Zaire. Following treatment, a quick re-infection can be observed if no measures are taken to reduce transmission. It is shown that the rate of re-infection is reduced when the water bodies around an endermc village are properly molluscrcrded. When. in addltlon to chemotherapy. a strategy of focal mollusciciding was adopted beneficial effects were visible I2 months after treatment but no longer at 20 months. In view of the comparatively small size of the human populations in the endemic villages, and due to the extent and the variety of the snail-infested water bodies. chemotherapy only, without additional measures. would seem to be the most cost-effective type control, under the prevailing conditions. This conclusion should be revised when long term health-planning could be effectively envisaged for the area.
of
ITVTRODUCTIOiX
agreed upon that the most effective way to control schistosomiasis is a system of integrated control in which all possible means of control are combined. In such a control effort. snail control is supplemented by measures to reduce the rate of snails to become infected by implementing sanitary measures. The other key-stone of this type of control, treatment of the infected subjects, is supplemented by measures to minimize re-infection of man: safe water is provided and barriers are constructed to prevent man from contact with infested water. When financial constraints exist, the question becomes pertinent which of the possible measures of control are the most effective, the cheapest and the most acceptable to the infected population. This should be considered both on the long run and on the short. And this question should be answered, without any doubt, in different ways for different areas, depending on the features of the area. In the present paper. it will be attempted to consider the aims of control in relation to the region’s development and to describe. more specifically, the implications of such considerations for the tin mining region of Maniema in Eastern Zaire. It is generally
THE PARASITE
The natural history of the parasite is characterized, as in many other parasitic diseases, by the production of an enormous offspring. In an illustrative example, Sturrock showed the reproductive potential of St Lucian S. r~ansoni to be 25,000.000,000 [ 11. One pair of adult schistosomes should be able to produce that many offspring. if no mortality among the free living stages and of the infected snails would occur. In most endemic areas. however, there is a relative stability in the parasite populations [2.3]. Except in situations of *Parts of this investigation received financial support from the UNDP:World Bank/WHO Special Programme for Research and Training in Tropical Diseases. ss3
19:1”-E
newly created habitats, prevalence and intensity of infection normally do not change dramatically in short periods of time. This implies that, in such stable situations, out of the 25 billion offspring, an average of two (one male and one female) will succeed to replace the parent generation. This type of observations has stimulated Bradley in his paper on the regulation of parasite populations, to conclude that parasite populations are not efficiently regulated by transmission factors only, in the case of schistosomiasis, and that other regulatory factors are very likely to exist [4]. The nature of those other factors, however, at the ‘host population level’ and at the ‘individual host level’. is not exactly understood, in schistosomiasis. THE EPIDEMIOLOGICAL PRESENTATIOK PARASITE
OF THE
Schistosomiasis is notoriously scattered in its distribution. Many of the earlier surveys stressed the feature; Bradley, in his general theory on the epidemiology and control of parasitic infections, paid a lot of attention to this aspect, and. more recently, the spatial characteristics have been introduced in a mathematical model [5]. In practice, this implies that over relatively short distances, the transmission pattern may vary enormously. More often than not it remains obscure to the layman’s eye, and even to many highly experienced eyes, which factors govern this particular distribution. Why is the parasite found in one part of the community and far less so in the other part? Why are some streams much more heavily infested than others in the same area? In Ethiopia it has been shown [6] how in the area North of Lake Tana, different types of snail ecology combined with different patterns of human behaviour. in three types of villages, could result in very similar prevalences of S. mansoni. In Maniema, Zaire, quantitative parasitological stool surveys have been made in a large number of villages [7]. There again, it is striking to note that two villages, Kakota and Amakinga, which are located a 1073
1074
A. M.
POLDERMAN
SETTING
I 100
km
Fig. I. Map of Maniema (Kivu Province, Zaire).
couple of kilometers apart, are infested to the same extent (Table I), although the level of transmission would seem altogether different. In Kakota, a manmade canal, harbouring vast numbers of Biomphalaria pfe[fJl?ri, crosses the centre of the village. In Amakinga, on the other hand, no such a focus of transmission is available; no snail can be found in the neighbourhood and clear household water is available in a noninfested stream just outside the village. These examples illustrate that within the limits of an endemic area, it remains very difficult to recognize the transmission patterns and to explain the level of infection, in terms of quality of snail-habitats, snail densities. water-contact behaviour, availability of alternative sources of water, excreta-disposal, etc. At the same time. it implies that the effect of intervention in these factors (which determine the intensity of transmission) is also very unpredictable. It implies that a thorough analysis of the local situation, and of the interrelationships of all factors in that particular area is required before the deliberate change by man of a small part of this complex of transmission factors, is likely to result in successful control. An ecosystem and a way of life have to be changed to be sure of lasting effect on the parasites’ natural history. From a financial point of view, this is not an inviting task.
OF
Kakota (n)
Makundju (n)
Amakinga (fl)
(n)
(YO I
I I4
(1x6)
I54
(17)
236
4x2
11041
644
(821
901
( 103)
256
(46)
9XX
1139)
602
(4X)
I ox’)
75x
(24)
596
716 440
YX3
(39)
57x
(2.1)
302
1x6) (l3Y)
135)
(83)
575
(55)
360
234
(IX21
2YH
(77) 1x41
440
(X5)
1x0
(23) (401
?o() -7, -_-
II631
334
(X4)
41x
(X4)
864
(35)
(Ilhl
?I6
(X2)
453
(27)
426
131)
I I4
1361
RESEARCH
PROJECT
In Maniema (Kivu Province, Eastern ZaireI. schistosomiasis due to S. /~c~ern~~rohi~~l and S. intercalaturn has been described to occur along the shores of the river Lualaba more than 40 years ago [&I 11. Schistosoma mansoni. however. did not occur in the rain forest to the east of Kindu. The latter area was scarcely populated and consisted of almost uninterrupted primary rain forests until about 1932. Then, economic development started: ecologic conditions gradually changed and intestinal schistosomiasis became endemic. The course of events which led to settlement and explosive increase of endemic schistosomiasis has been described elsewhere in more detail [7]. In short, the exploitation of open tin mines started in 1932, but it was not until the end of the Second World War that extensive systems to provide water into the exploitations were required. To that purpose. several man-made lakes were created and canals were dug to transport the water from the lakes into the open mines. Parallel with the construction of these waterworks. semi-permanent villages were constructed for the labourers and their families. The size of these minmg villages vary from 100 to about 2000 inhabitants. Following the creation of the man-made lakes. the first cases of autochtonous intestinal schistosomiasis were reported around 1956. Apparently it was not until the middle of the 1960s that an explosive increase 01 schistosomiasis in the area was observed [7. 121. At present, the situation is such that in many of the mining villages of the Soci&tt Minitre et Industrielle de Kivu (SOMINKI), both the prevalence and the intensity of infection are extremely high. Some selected data on the endemicity of schistosomiasis in the area are summarized in Table I. In other communities however, schistosome infections are rare and limited to imported infections from the infested communities [7 1. The endemic and non-endemic communities are located closely together and no differences in economic or social way oflife could be recognized. The presence or absence of schistosomiasis would seem to depend on geological and hydrobiological features and on characteristics of the exploitation. The great similarity of both types of villages in many aspects. but the presence of schistosomlasis. offers attractive prospects for research.
REGONS
Tshamaka
THE
FOR
CONTROL
There are several reasons why schistosomiasis is believed to be a serious disease in Muniema. and why control is considered to have some priority. The first argument why some sort of control might be needed is the fact that prevalence and egg count levels are extremely high, in many communities. These simple parasitological observations suggest that schistosomiasis might be a serious disease in this area (Table
11. The second. and even more direct indicator that schistosomiasis is a serious disease worth to be controlled in the area. is the clinical observation that the infected subjects are physically affected. In the heavily infested villages, the mean hepatomegalyand increased as splenomegaly-rates are signifcantly
Controlling
intestmai
compared with the non-endemic villages (unpublished data). This is illustrated in Fig. 2. The third indication of the severity of schistosomiasis in the area refers to the frequency of complaints. In an inquiry in a heavily infested and in a non-endemic community. large differences in the types of complaints were observed [ 131. Intermittent and bloody diarrhoea were complained of by about half of the subjects in the infested community and were almost non-existent in the non-endemic village. ‘Abdominal discomfort’ was 2-3 times more common in the infested village and ‘fatigue’ was mentioned about 4 times more often among children in the infested village. The next reason for control should have been the result of observations on decreased productivity in manual labour and increased absenteeism in infected labourers. Although the conditions are favourable to demonstrate this type of differences between the subjects in endemic and non-endemic villages, results are not yet available. A last reason to believe that schistosomiasis control would urgently be needed in Maniema. could be the demonstration of decreased physical fitness in ergometric tests. in the endemic villages. Both step tests and bicycle ergometric tests have been carried out in endemic and non-endemic villages, but no difference could be found [14].
LUEI
schistosomiasis
1075
Although the impact of the disease on man’s physical fitness and productivity could not be demonstrated properly as yet, the first three factors (egg counts, hepatomegaly, complaints) clearly demonstrate that the infections are heavier and the signs and symptoms more pronounced than in a great majority of other endemic areas. Consequently schistosomiasis control is thought to be of great importance to the health of the resident population. CONTROL EFFORTS
Due to the diversity and extent of the snail-infested water bodies, snail control is considered to be difficult to achieve and very expensive to carry out, in the tmmining region of Maniema. This is particularly so because the number of persons protected by these measures is mostly small as a result of the small size of the villages. Since the total population at risk of serious infection is also limited (+- lS,OOO), it was attempted to achieve control of the disease primarily through chemotherapy of the human population. The control measures, therefore, did not primarily aim at control of transmission and certainly not at partial eradication, but rather at disease control. The degree of success of the control measures ought to be expressed, therefore, in terms of improvement of the clinical picture (decrease of hepatomegaly or
742
LE
NIABESI
s97
TSHONKA
506
TSHAMAKA KAKOTA AMAKINGA UNGBE MAKUNDJU YUBULI ISONGO TEMBO BENGO MASI
II MEL0
BATAMBA AVUANGA AMEKUPI
IOCOI 1ty
m
PREVALENCE
prevalence percentage ercretlng
AND
INTENSITY
Of Smanson, Of mpre
pOpUlQtlOn than 600
OF
INFECTION
lnfectlons
epg
n
HEPATOMEGALY
m
Ilver pdpoble cost01 morgl” ltver below
5cm or Cost01
SPLENOMEGALY
below
more margin
spleen
Fig. 2. Prevalence and intensity of infection and hepatomegaly and splenomegaly rates in heavily infested and non-endemic villages of Maniema’s tin-mining area.
2
3
A. M. POLDERMAL
1076 % frequency
age In year
of egg counts
2-i
Fig. 3. Frequency
distribution Tshamaka.
of eggcounts before and 6 weeks after treatment with oxamniquine m pretreatment count: m posttreatment count.
splenomegaly) or of the improvement of the ‘quality of life’ (e.g. as a reduction of the number and intensity of complaints). These parameters, however. are not commonly used. and subject to many biases. For the time being, therefore. egg counts were used as the sole measure to quantify parasitological infection and to record improvement after treatment. Following some trials with chemotherapy with low doses of hycanthone [IS], this drug is now abandoned and replaced by oxamniquine (I5 or 40mg.!kg) and praziquantel (40 mg,kg). Since the dose response varies enormously in treatment with oxamniquine [I(,]. the proper dose of this drug to be used in Maniema had to be determined at first. To this purpose randomly selected terciles of the population of some communities (e.g. Tshamaka) were treated either with I5 or 40 mg;kg of oxamniquine or with a placebo. The effect of treatment is visualized by plotting the frequency dlstributlon 01’ egg counts before and 6 weeks after treatment in one tigure. This is done for 5 diRerent age groups (Fig. 3*). It can be seen that the results of treatment are better in adults than in children. and that the ‘cure rates’ are much higher in the 4Omg:kg group. For individual climcal use, 15 mgikg would seem insutticient in this area. This does not necessarily mean that I5 mg,‘kg is too low a dose for use in a control programme. Subsequently. lhc intcnslty of infection wah rc-
in
corded at I), 4.8. 12 and 20 months after treatment for all who received treatment. During these follow-up studies. it was observed that many eggs were excreted again a few months after treatment. In order to reduce this rate of reappearance of eggs. it was tried to reduce transmission as well. This was done in two different ways. In one village (Makundju). svstematic snail control was aimed at in all water bodies in the direct environment of the village up to a distance of several kilometers outside the village. In the other village (Kakota), only the principal and very obvious transmission site was treated frequently and thoroughly. In this village. a heavily infested canal passes the centre ofthevillage and a large part ofall water contacts takes place along this canal. The shores of the lake. the marshes and various smaller water contact points all located farther away were left untreated. There. transmission could go on. It should be notod that for a number of reasons quite some people wcrc not treated. Chemotherapy aimed at reducing worm burdens in indlvlduals and not at interrupting or cvcn clTectively reducing transmission. The etl’ect of treatment IS graphically presented m two different ways. At first (Fig. 4). the age-specific percentage reduction OI- lncrcase In egg counts of all treated subjects is given at I7 and a! 20 months after treatment. It can be obscrvcd that reappearance 01 eggs IS very quick in Tshamaha (chemotherapy only). slower in Kukota and the slov+cst In Makundju (chemotherapy + intcnsc snarl control). The tigurc
Controlling
intestinal
schistosomiasis
\
4
A
:\::y_-
\ _-
60
-n- ------__&
Fig. 4.(A)Age specific change of the geometric mean egg counts following treatment with oxamniquine, 15mg!kg. n 12 months: A 20 months after treatnient.
Fig. 4.(B)Age specific change of the geometric mean egg counts following treatment with oxamniquine. 40 mg/kg.
also shows that there is no gross difference in the rate of reappearance of eggs when both treatment schedules ( IS or 40 mg ‘kg) are compared. Then the percentages who excrete over 600 eggs,g before treatment’and who do so at 17months (Fig. 5A) or at 20 months (Fig. 5B) after treatment. are plotted. In this figure only those who were both examined before treatment and treated and re-examined afterwards. are taken into account. The level of 600 eggs g was chosen because above this-arbitrary-level. renewed treatment was considered necessary. The figures shoH- that: (I ) There is little advantage in using the expensive
high dose of oxamniquine even though at 6 weeks the lower gose might seem insufficient. (2) Re-appearance of eggs is very quick in Tshamaka. (3) A lot of transmission would seem to be still going on in Kakota. Taking away the most important transmission site seemed to be effective at the 12 months survey. but at 20 months the effect had almost disappeared. (4) Even at Makundju-although at a much lower level-re-infection seems to occur. (5) The reappearance of eggs is more pronounced in the younger age groups than in the older ones.
a
12 months:
A 20 months
after treatment.
A. M.
POLDERMAN
.
A
TSHAMAKA
. . . . ...“‘&\
: :
‘...
:
\
10
20
40
60
‘...
A ... ~~*....__ .*.-.-
.
...._______*_A
!
5
\
..
: ;:
5
10
20
40
60
80 %
.e*’ 60 %
A.
1 ..._
“...
KAKDTA
. . ...
I
*..*
:--_A
j’ 40 $ I
i
P
20 % .
..
‘\
\
\
*-.-..a -..._ 5_._..
-....--.___
\ \ \
I
\-__---I
0
Fig. S(A)Age-specific percentage of subjects who excrete more than 600 eggs/g. For each of the three villages the situation before (A .‘.... A) and 12 months after (A - - A) intervention are compared.
Fig. 5.(B)Age-specific percentages of subjects who excrete more than 600 eggs/g. For each of the v~llagrs the situation before (A......A) and 20 months after (A ~A) intervention are compared.
It must be stressed that it can not be concluded that observed differences are caused by the different types of intervention. The pretreatment levels of egg counts were not exactly the same, and the intensity of transmission was undoubtedly different. Even with identical types of intervention, the rate of reappearance of eggs might have been quite different. It can only be observed that the three study-villages were all highly infected and that in each of them intense transmission took place in the canals crossing or closely passing the village.
On the short term. not looking ahead more than 20 months. and assessing the effort of intervention in terms of egg counts only. chemotherapy without additional snail control did result in the need of greater numbers of new treatments than the combinaiion of chemotherapy plus snail control. The difference. however, was not very great in the case of focal snail control (Kakota). while the measures to achieve
the
Finunicd
aspects
oj the control
ejjtirts
If an egg excretion of 600 eggs/g would be adopted as a threshold above which treatment of a subject is required again, even in Makundju a lot of children need to be treated again at 20 months. The cost of required drugs per capita can be calculated for each of the three villages. If one capsule of oxamniquine (250 mg) is supposed to cost $I, when the I5 mg/kg dose is used, and when we allow for the existing age distribution and the low average weight of the local population, the cost of required drugs could be calculated as summarized in Table 2.
Controlling
intestinal
intense snail control (Makundju) required a great deal of organization and supervision and large quantities of bayluscide. TOWARDS
A STRATEGY
OF CONTROL
The economic situation in present day Zaire is not a promising one. The majority of potentially rich mining companies are making losses and the infra-structure of the country is such that enormous investments would be necessary to change this. As a consequence little is invested in the existing mining companies and long term development is replaced by short term planning. In schistosomiasis control. too, there is a great reluctance to implement costly measures which aim at changing transmission in the long run. Yet. measures are badly needed at this moment, as pointed out in the previous paragraphs. In this context it would seem realistic to base the system of control on the results obtained during a relatively short period of evaluation (12-20 months only). The parasitological results suggest that in Maniema. in an area with many different types of infested water bodies and with small pockets of human population. repeated treatment of the heavily infested population is the most cost effective way ofcontrol and that focal snail control ought to be added only to such extent. that it does not greatly add to the costs of intervention. This conclusion. however, depends on a few assumptions: It depends on the availability of a mobile field team (personnel plus vehicle) to examine and treat the population. It assumes that the observed reductions in egg counts properly reflects reduced morbidity in the population and reduced disease in the individual. It is based on the small magnitude of the mining villages in comparison with the numbers and sizes of snail-infested water bodies. It depends on the time scale for which measures are considered. As soon as planning is oriented for a longer period ahead. the conclusion should be reconsidered. It is based on the observation that the social structure of the mining villages is not such that effective participation of the population in the organization of snail control can be envisaged. The conclusion is the condensation of a parasitologist’s experience and his most cost-effective suggestion to quite a particular type of decisionmaker: to a mining company. Schistosomiasis control, however. is not only a matter of how to deal with ill people in the cheapest and most cost-effective way. It is also a manifestation of development and of an increased awareness of both decision-maker and the population for man’s health. To further develop this awareness. participation of the infected population in activities to control serious schistosomiasis is ofcrucial importance. A strategy of control that ignores the development of the population’s awareness of the risk of transmission and that ignores the importance of their participation in control. is unacceptable from a public health point of view. Whether additional measures like partial snail control. building of latrines, provision of safe water and drainage of infested marshes will soon result in recognisable reduction of
schistosomiasis
1079
prevalence. intensity of infection and reduction of the rate of re-infection following chemotherapy, remains doubtful. It is more likely that their impact will become visible primarily in a very general and diffuse way. They are a manifestation of development of a public health awareness. a development of which the organization of mass treatment for schistosomiasis is another exponent, rather than a direct and efficient way of schistosomiasis control. In short, and very practically: population-based chemotherapy should be the first and most important way ofcontrol in the area. Focal snail control has to be added in those communities where the most obvious and important transmission sites can be molluscicided at comparatively low costs and other measures ought to be taken to mobilize the people’s awareness and to visualize that repeated chemotherapeutic treatments are a part of an integrated approach towards a healthier life in Maniema. The parasitologist’s most cost-effective tool to reduce egg counts of schistosomes in tin-mine labourers, is not the only type of consideration upon which to base a control programme. Indeed, 25 years after the introduction of schistosomiasis into the area, we cannot afford to shirk the uninviting task of changing an ecosystem and a way of life once again. Acknor,ledgemenrs-The research on which the present paper is based has been carried out in close cooperation with a great number of others. 1 wish to acknowledge in particular the work of Kayiteshonga Mpamila. leader of the field team. Amissie Sumailie, Wisenga Bwalagwa and Wabenga Butelezi. members ofthe field team, Dr J. L. Gerold and Mr H. de Vries of the Laboratory of Parasitology in Leiden. Mrs BouwhuisHoogerwerf of the Department of Medical Statistics of the Leiden University, Dr B. Gryseels, Ministry of Health Bujumbura and Dr J. P. Manshande. former Medical Director of the SOMINKI hospital in Kalima. Zaire. REFERENCES
I. Sturrock R. F. Problems associated with mollusciciding natural habitats. In Molluscicides in Schisrosomiasrs Control (Edited by Cheng T. C.), pp. 51-65. Academic Press, London, 1974. F. S. and Bradley D. J. Egg output stability 2. McCullough and the epidemiology of Schistosoma haematobium. Part 1. Variations and stability in Schistosoma haematobium egg counts. Trans. R. Sot. rrop. Med. Hyg. 67,475-490, 1973. and stability in 3. Wilkins H. A. and Scott A. Variation Schistosoma haematobium egg counts: a four-year study of Gambian children. Trans. R. Sot. trop. Med. Hyg. 72, 397-404, 1978. 4. Bradley D. J. Regulation of parasite population. Trans. R. Sot. trop. Med. Hyg. 66, 697-708, 1972. of helminth 5. Bradley D. J. and May R. M. Consequences aggregation for the dynamics of Schistosomiasis. Trans. R. Sot. trop. Med. Hyg, 72, 262, 1978. 6. Polderman A. M. The transmission of intestinal Schistosomiasis in Begemer province, Ethiopia. Thesis. Leiden, 1975. I. Polderman A. M. et al. Intestinal schistosomiasis in the mining district of Maniema. Kivu province. Zaire. Parts 1 and 2. Annls Sot. beige Med. trap. Accepted for publication. 8. Chesterman C. Note sur la bilharziose dans la region de Stanleyville (Congo Belge). Ann/s Sot. helge M&d. frop. 3, 73-76, 1923. 9. Fisher A. C. A study of the schistosomiasis of the
1080
10.
I I. 12. 13.
A. M. POLDERMAN
Stanleyville district of the Belgian Congo. Trans. R. Sot. trap. IVied. Hyg. Zg, 277-306. 1934. Berghe L. van den Les schtstosomes et les schistosomoses au Congo Belge et dans les territoires du RuandaUrundi. Institute Royal Colonial Beige, MemoiresCollection. 1939. Gillet J. and Wolfs J. Les bilharzioses humaines au Congo Belge et au Ruanda-Urundi. Bull. Wld Hlrh Org. 10,315-419, 1954. Schyns Ch. Personal communication. Polderman A. M., Kayiteshonga Mpamila, Manshande J. P.. Gerold J. L.. De Vries H. and Gryseels B. On the
distribution and control of schtstosomiasis mansom in Maniema. Zaire. Acta Leidensia 49. 17-29. I98 I. 14. Ee J. H. van and Polderman A. M. Physiologtcal performance and work capacity of tin mme labourers m Zaire infested with schistosomiasis. Twp. gqy. .Jfud. Accepted for publication. 15. Polderman A. M. and Manshande J. P. Futlure of targeted mass treatment to control schtstosomtasis. Lancer 3 January, 1981. 16. Epidemiology and control ofschistosomtasis. Report ofa WHO Expert Committee. WHO Technical Report Series No. 643.
for Parasitology,
State University
POLDERMAN
of Leiden. Wassenaarweweg
62, Leiden. The Netherlands
Abstract-Intestinal schistosomiasis is highly prevalent among the labourers and their families in many of the miners’ villages in Maniema, Zaire. Following treatment, a quick re-infection can be observed if no measures are taken to reduce transmission. It is shown that the rate of re-infection is reduced when the water bodies around an endermc village are properly molluscrcrded. When. in addltlon to chemotherapy. a strategy of focal mollusciciding was adopted beneficial effects were visible I2 months after treatment but no longer at 20 months. In view of the comparatively small size of the human populations in the endemic villages, and due to the extent and the variety of the snail-infested water bodies. chemotherapy only, without additional measures. would seem to be the most cost-effective type control, under the prevailing conditions. This conclusion should be revised when long term health-planning could be effectively envisaged for the area.
of
ITVTRODUCTIOiX
agreed upon that the most effective way to control schistosomiasis is a system of integrated control in which all possible means of control are combined. In such a control effort. snail control is supplemented by measures to reduce the rate of snails to become infected by implementing sanitary measures. The other key-stone of this type of control, treatment of the infected subjects, is supplemented by measures to minimize re-infection of man: safe water is provided and barriers are constructed to prevent man from contact with infested water. When financial constraints exist, the question becomes pertinent which of the possible measures of control are the most effective, the cheapest and the most acceptable to the infected population. This should be considered both on the long run and on the short. And this question should be answered, without any doubt, in different ways for different areas, depending on the features of the area. In the present paper. it will be attempted to consider the aims of control in relation to the region’s development and to describe. more specifically, the implications of such considerations for the tin mining region of Maniema in Eastern Zaire. It is generally
THE PARASITE
The natural history of the parasite is characterized, as in many other parasitic diseases, by the production of an enormous offspring. In an illustrative example, Sturrock showed the reproductive potential of St Lucian S. r~ansoni to be 25,000.000,000 [ 11. One pair of adult schistosomes should be able to produce that many offspring. if no mortality among the free living stages and of the infected snails would occur. In most endemic areas. however, there is a relative stability in the parasite populations [2.3]. Except in situations of *Parts of this investigation received financial support from the UNDP:World Bank/WHO Special Programme for Research and Training in Tropical Diseases. ss3
19:1”-E
newly created habitats, prevalence and intensity of infection normally do not change dramatically in short periods of time. This implies that, in such stable situations, out of the 25 billion offspring, an average of two (one male and one female) will succeed to replace the parent generation. This type of observations has stimulated Bradley in his paper on the regulation of parasite populations, to conclude that parasite populations are not efficiently regulated by transmission factors only, in the case of schistosomiasis, and that other regulatory factors are very likely to exist [4]. The nature of those other factors, however, at the ‘host population level’ and at the ‘individual host level’. is not exactly understood, in schistosomiasis. THE EPIDEMIOLOGICAL PRESENTATIOK PARASITE
OF THE
Schistosomiasis is notoriously scattered in its distribution. Many of the earlier surveys stressed the feature; Bradley, in his general theory on the epidemiology and control of parasitic infections, paid a lot of attention to this aspect, and. more recently, the spatial characteristics have been introduced in a mathematical model [5]. In practice, this implies that over relatively short distances, the transmission pattern may vary enormously. More often than not it remains obscure to the layman’s eye, and even to many highly experienced eyes, which factors govern this particular distribution. Why is the parasite found in one part of the community and far less so in the other part? Why are some streams much more heavily infested than others in the same area? In Ethiopia it has been shown [6] how in the area North of Lake Tana, different types of snail ecology combined with different patterns of human behaviour. in three types of villages, could result in very similar prevalences of S. mansoni. In Maniema, Zaire, quantitative parasitological stool surveys have been made in a large number of villages [7]. There again, it is striking to note that two villages, Kakota and Amakinga, which are located a 1073
1074
A. M.
POLDERMAN
SETTING
I 100
km
Fig. I. Map of Maniema (Kivu Province, Zaire).
couple of kilometers apart, are infested to the same extent (Table I), although the level of transmission would seem altogether different. In Kakota, a manmade canal, harbouring vast numbers of Biomphalaria pfe[fJl?ri, crosses the centre of the village. In Amakinga, on the other hand, no such a focus of transmission is available; no snail can be found in the neighbourhood and clear household water is available in a noninfested stream just outside the village. These examples illustrate that within the limits of an endemic area, it remains very difficult to recognize the transmission patterns and to explain the level of infection, in terms of quality of snail-habitats, snail densities. water-contact behaviour, availability of alternative sources of water, excreta-disposal, etc. At the same time. it implies that the effect of intervention in these factors (which determine the intensity of transmission) is also very unpredictable. It implies that a thorough analysis of the local situation, and of the interrelationships of all factors in that particular area is required before the deliberate change by man of a small part of this complex of transmission factors, is likely to result in successful control. An ecosystem and a way of life have to be changed to be sure of lasting effect on the parasites’ natural history. From a financial point of view, this is not an inviting task.
OF
Kakota (n)
Makundju (n)
Amakinga (fl)
(n)
(YO I
I I4
(1x6)
I54
(17)
236
4x2
11041
644
(821
901
( 103)
256
(46)
9XX
1139)
602
(4X)
I ox’)
75x
(24)
596
716 440
YX3
(39)
57x
(2.1)
302
1x6) (l3Y)
135)
(83)
575
(55)
360
234
(IX21
2YH
(77) 1x41
440
(X5)
1x0
(23) (401
?o() -7, -_-
II631
334
(X4)
41x
(X4)
864
(35)
(Ilhl
?I6
(X2)
453
(27)
426
131)
I I4
1361
RESEARCH
PROJECT
In Maniema (Kivu Province, Eastern ZaireI. schistosomiasis due to S. /~c~ern~~rohi~~l and S. intercalaturn has been described to occur along the shores of the river Lualaba more than 40 years ago [&I 11. Schistosoma mansoni. however. did not occur in the rain forest to the east of Kindu. The latter area was scarcely populated and consisted of almost uninterrupted primary rain forests until about 1932. Then, economic development started: ecologic conditions gradually changed and intestinal schistosomiasis became endemic. The course of events which led to settlement and explosive increase of endemic schistosomiasis has been described elsewhere in more detail [7]. In short, the exploitation of open tin mines started in 1932, but it was not until the end of the Second World War that extensive systems to provide water into the exploitations were required. To that purpose. several man-made lakes were created and canals were dug to transport the water from the lakes into the open mines. Parallel with the construction of these waterworks. semi-permanent villages were constructed for the labourers and their families. The size of these minmg villages vary from 100 to about 2000 inhabitants. Following the creation of the man-made lakes. the first cases of autochtonous intestinal schistosomiasis were reported around 1956. Apparently it was not until the middle of the 1960s that an explosive increase 01 schistosomiasis in the area was observed [7. 121. At present, the situation is such that in many of the mining villages of the Soci&tt Minitre et Industrielle de Kivu (SOMINKI), both the prevalence and the intensity of infection are extremely high. Some selected data on the endemicity of schistosomiasis in the area are summarized in Table I. In other communities however, schistosome infections are rare and limited to imported infections from the infested communities [7 1. The endemic and non-endemic communities are located closely together and no differences in economic or social way oflife could be recognized. The presence or absence of schistosomiasis would seem to depend on geological and hydrobiological features and on characteristics of the exploitation. The great similarity of both types of villages in many aspects. but the presence of schistosomlasis. offers attractive prospects for research.
REGONS
Tshamaka
THE
FOR
CONTROL
There are several reasons why schistosomiasis is believed to be a serious disease in Muniema. and why control is considered to have some priority. The first argument why some sort of control might be needed is the fact that prevalence and egg count levels are extremely high, in many communities. These simple parasitological observations suggest that schistosomiasis might be a serious disease in this area (Table
11. The second. and even more direct indicator that schistosomiasis is a serious disease worth to be controlled in the area. is the clinical observation that the infected subjects are physically affected. In the heavily infested villages, the mean hepatomegalyand increased as splenomegaly-rates are signifcantly
Controlling
intestmai
compared with the non-endemic villages (unpublished data). This is illustrated in Fig. 2. The third indication of the severity of schistosomiasis in the area refers to the frequency of complaints. In an inquiry in a heavily infested and in a non-endemic community. large differences in the types of complaints were observed [ 131. Intermittent and bloody diarrhoea were complained of by about half of the subjects in the infested community and were almost non-existent in the non-endemic village. ‘Abdominal discomfort’ was 2-3 times more common in the infested village and ‘fatigue’ was mentioned about 4 times more often among children in the infested village. The next reason for control should have been the result of observations on decreased productivity in manual labour and increased absenteeism in infected labourers. Although the conditions are favourable to demonstrate this type of differences between the subjects in endemic and non-endemic villages, results are not yet available. A last reason to believe that schistosomiasis control would urgently be needed in Maniema. could be the demonstration of decreased physical fitness in ergometric tests. in the endemic villages. Both step tests and bicycle ergometric tests have been carried out in endemic and non-endemic villages, but no difference could be found [14].
LUEI
schistosomiasis
1075
Although the impact of the disease on man’s physical fitness and productivity could not be demonstrated properly as yet, the first three factors (egg counts, hepatomegaly, complaints) clearly demonstrate that the infections are heavier and the signs and symptoms more pronounced than in a great majority of other endemic areas. Consequently schistosomiasis control is thought to be of great importance to the health of the resident population. CONTROL EFFORTS
Due to the diversity and extent of the snail-infested water bodies, snail control is considered to be difficult to achieve and very expensive to carry out, in the tmmining region of Maniema. This is particularly so because the number of persons protected by these measures is mostly small as a result of the small size of the villages. Since the total population at risk of serious infection is also limited (+- lS,OOO), it was attempted to achieve control of the disease primarily through chemotherapy of the human population. The control measures, therefore, did not primarily aim at control of transmission and certainly not at partial eradication, but rather at disease control. The degree of success of the control measures ought to be expressed, therefore, in terms of improvement of the clinical picture (decrease of hepatomegaly or
742
LE
NIABESI
s97
TSHONKA
506
TSHAMAKA KAKOTA AMAKINGA UNGBE MAKUNDJU YUBULI ISONGO TEMBO BENGO MASI
II MEL0
BATAMBA AVUANGA AMEKUPI
IOCOI 1ty
m
PREVALENCE
prevalence percentage ercretlng
AND
INTENSITY
Of Smanson, Of mpre
pOpUlQtlOn than 600
OF
INFECTION
lnfectlons
epg
n
HEPATOMEGALY
m
Ilver pdpoble cost01 morgl” ltver below
5cm or Cost01
SPLENOMEGALY
below
more margin
spleen
Fig. 2. Prevalence and intensity of infection and hepatomegaly and splenomegaly rates in heavily infested and non-endemic villages of Maniema’s tin-mining area.
2
3
A. M. POLDERMAL
1076 % frequency
age In year
of egg counts
2-i
Fig. 3. Frequency
distribution Tshamaka.
of eggcounts before and 6 weeks after treatment with oxamniquine m pretreatment count: m posttreatment count.
splenomegaly) or of the improvement of the ‘quality of life’ (e.g. as a reduction of the number and intensity of complaints). These parameters, however. are not commonly used. and subject to many biases. For the time being, therefore. egg counts were used as the sole measure to quantify parasitological infection and to record improvement after treatment. Following some trials with chemotherapy with low doses of hycanthone [IS], this drug is now abandoned and replaced by oxamniquine (I5 or 40mg.!kg) and praziquantel (40 mg,kg). Since the dose response varies enormously in treatment with oxamniquine [I(,]. the proper dose of this drug to be used in Maniema had to be determined at first. To this purpose randomly selected terciles of the population of some communities (e.g. Tshamaka) were treated either with I5 or 40 mg;kg of oxamniquine or with a placebo. The effect of treatment is visualized by plotting the frequency dlstributlon 01’ egg counts before and 6 weeks after treatment in one tigure. This is done for 5 diRerent age groups (Fig. 3*). It can be seen that the results of treatment are better in adults than in children. and that the ‘cure rates’ are much higher in the 4Omg:kg group. For individual climcal use, 15 mgikg would seem insutticient in this area. This does not necessarily mean that I5 mg,‘kg is too low a dose for use in a control programme. Subsequently. lhc intcnslty of infection wah rc-
in
corded at I), 4.8. 12 and 20 months after treatment for all who received treatment. During these follow-up studies. it was observed that many eggs were excreted again a few months after treatment. In order to reduce this rate of reappearance of eggs. it was tried to reduce transmission as well. This was done in two different ways. In one village (Makundju). svstematic snail control was aimed at in all water bodies in the direct environment of the village up to a distance of several kilometers outside the village. In the other village (Kakota), only the principal and very obvious transmission site was treated frequently and thoroughly. In this village. a heavily infested canal passes the centre ofthevillage and a large part ofall water contacts takes place along this canal. The shores of the lake. the marshes and various smaller water contact points all located farther away were left untreated. There. transmission could go on. It should be notod that for a number of reasons quite some people wcrc not treated. Chemotherapy aimed at reducing worm burdens in indlvlduals and not at interrupting or cvcn clTectively reducing transmission. The etl’ect of treatment IS graphically presented m two different ways. At first (Fig. 4). the age-specific percentage reduction OI- lncrcase In egg counts of all treated subjects is given at I7 and a! 20 months after treatment. It can be obscrvcd that reappearance 01 eggs IS very quick in Tshamaha (chemotherapy only). slower in Kukota and the slov+cst In Makundju (chemotherapy + intcnsc snarl control). The tigurc
Controlling
intestinal
schistosomiasis
\
4
A
:\::y_-
\ _-
60
-n- ------__&
Fig. 4.(A)Age specific change of the geometric mean egg counts following treatment with oxamniquine, 15mg!kg. n 12 months: A 20 months after treatnient.
Fig. 4.(B)Age specific change of the geometric mean egg counts following treatment with oxamniquine. 40 mg/kg.
also shows that there is no gross difference in the rate of reappearance of eggs when both treatment schedules ( IS or 40 mg ‘kg) are compared. Then the percentages who excrete over 600 eggs,g before treatment’and who do so at 17months (Fig. 5A) or at 20 months (Fig. 5B) after treatment. are plotted. In this figure only those who were both examined before treatment and treated and re-examined afterwards. are taken into account. The level of 600 eggs g was chosen because above this-arbitrary-level. renewed treatment was considered necessary. The figures shoH- that: (I ) There is little advantage in using the expensive
high dose of oxamniquine even though at 6 weeks the lower gose might seem insufficient. (2) Re-appearance of eggs is very quick in Tshamaka. (3) A lot of transmission would seem to be still going on in Kakota. Taking away the most important transmission site seemed to be effective at the 12 months survey. but at 20 months the effect had almost disappeared. (4) Even at Makundju-although at a much lower level-re-infection seems to occur. (5) The reappearance of eggs is more pronounced in the younger age groups than in the older ones.
a
12 months:
A 20 months
after treatment.
A. M.
POLDERMAN
.
A
TSHAMAKA
. . . . ...“‘&\
: :
‘...
:
\
10
20
40
60
‘...
A ... ~~*....__ .*.-.-
.
...._______*_A
!
5
\
..
: ;:
5
10
20
40
60
80 %
.e*’ 60 %
A.
1 ..._
“...
KAKDTA
. . ...
I
*..*
:--_A
j’ 40 $ I
i
P
20 % .
..
‘\
\
\
*-.-..a -..._ 5_._..
-....--.___
\ \ \
I
\-__---I
0
Fig. S(A)Age-specific percentage of subjects who excrete more than 600 eggs/g. For each of the three villages the situation before (A .‘.... A) and 12 months after (A - - A) intervention are compared.
Fig. 5.(B)Age-specific percentages of subjects who excrete more than 600 eggs/g. For each of the v~llagrs the situation before (A......A) and 20 months after (A ~A) intervention are compared.
It must be stressed that it can not be concluded that observed differences are caused by the different types of intervention. The pretreatment levels of egg counts were not exactly the same, and the intensity of transmission was undoubtedly different. Even with identical types of intervention, the rate of reappearance of eggs might have been quite different. It can only be observed that the three study-villages were all highly infected and that in each of them intense transmission took place in the canals crossing or closely passing the village.
On the short term. not looking ahead more than 20 months. and assessing the effort of intervention in terms of egg counts only. chemotherapy without additional snail control did result in the need of greater numbers of new treatments than the combinaiion of chemotherapy plus snail control. The difference. however, was not very great in the case of focal snail control (Kakota). while the measures to achieve
the
Finunicd
aspects
oj the control
ejjtirts
If an egg excretion of 600 eggs/g would be adopted as a threshold above which treatment of a subject is required again, even in Makundju a lot of children need to be treated again at 20 months. The cost of required drugs per capita can be calculated for each of the three villages. If one capsule of oxamniquine (250 mg) is supposed to cost $I, when the I5 mg/kg dose is used, and when we allow for the existing age distribution and the low average weight of the local population, the cost of required drugs could be calculated as summarized in Table 2.
Controlling
intestinal
intense snail control (Makundju) required a great deal of organization and supervision and large quantities of bayluscide. TOWARDS
A STRATEGY
OF CONTROL
The economic situation in present day Zaire is not a promising one. The majority of potentially rich mining companies are making losses and the infra-structure of the country is such that enormous investments would be necessary to change this. As a consequence little is invested in the existing mining companies and long term development is replaced by short term planning. In schistosomiasis control. too, there is a great reluctance to implement costly measures which aim at changing transmission in the long run. Yet. measures are badly needed at this moment, as pointed out in the previous paragraphs. In this context it would seem realistic to base the system of control on the results obtained during a relatively short period of evaluation (12-20 months only). The parasitological results suggest that in Maniema. in an area with many different types of infested water bodies and with small pockets of human population. repeated treatment of the heavily infested population is the most cost effective way ofcontrol and that focal snail control ought to be added only to such extent. that it does not greatly add to the costs of intervention. This conclusion. however, depends on a few assumptions: It depends on the availability of a mobile field team (personnel plus vehicle) to examine and treat the population. It assumes that the observed reductions in egg counts properly reflects reduced morbidity in the population and reduced disease in the individual. It is based on the small magnitude of the mining villages in comparison with the numbers and sizes of snail-infested water bodies. It depends on the time scale for which measures are considered. As soon as planning is oriented for a longer period ahead. the conclusion should be reconsidered. It is based on the observation that the social structure of the mining villages is not such that effective participation of the population in the organization of snail control can be envisaged. The conclusion is the condensation of a parasitologist’s experience and his most cost-effective suggestion to quite a particular type of decisionmaker: to a mining company. Schistosomiasis control, however. is not only a matter of how to deal with ill people in the cheapest and most cost-effective way. It is also a manifestation of development and of an increased awareness of both decision-maker and the population for man’s health. To further develop this awareness. participation of the infected population in activities to control serious schistosomiasis is ofcrucial importance. A strategy of control that ignores the development of the population’s awareness of the risk of transmission and that ignores the importance of their participation in control. is unacceptable from a public health point of view. Whether additional measures like partial snail control. building of latrines, provision of safe water and drainage of infested marshes will soon result in recognisable reduction of
schistosomiasis
1079
prevalence. intensity of infection and reduction of the rate of re-infection following chemotherapy, remains doubtful. It is more likely that their impact will become visible primarily in a very general and diffuse way. They are a manifestation of development of a public health awareness. a development of which the organization of mass treatment for schistosomiasis is another exponent, rather than a direct and efficient way of schistosomiasis control. In short, and very practically: population-based chemotherapy should be the first and most important way ofcontrol in the area. Focal snail control has to be added in those communities where the most obvious and important transmission sites can be molluscicided at comparatively low costs and other measures ought to be taken to mobilize the people’s awareness and to visualize that repeated chemotherapeutic treatments are a part of an integrated approach towards a healthier life in Maniema. The parasitologist’s most cost-effective tool to reduce egg counts of schistosomes in tin-mine labourers, is not the only type of consideration upon which to base a control programme. Indeed, 25 years after the introduction of schistosomiasis into the area, we cannot afford to shirk the uninviting task of changing an ecosystem and a way of life once again. Acknor,ledgemenrs-The research on which the present paper is based has been carried out in close cooperation with a great number of others. 1 wish to acknowledge in particular the work of Kayiteshonga Mpamila. leader of the field team. Amissie Sumailie, Wisenga Bwalagwa and Wabenga Butelezi. members ofthe field team, Dr J. L. Gerold and Mr H. de Vries of the Laboratory of Parasitology in Leiden. Mrs BouwhuisHoogerwerf of the Department of Medical Statistics of the Leiden University, Dr B. Gryseels, Ministry of Health Bujumbura and Dr J. P. Manshande. former Medical Director of the SOMINKI hospital in Kalima. Zaire. REFERENCES
I. Sturrock R. F. Problems associated with mollusciciding natural habitats. In Molluscicides in Schisrosomiasrs Control (Edited by Cheng T. C.), pp. 51-65. Academic Press, London, 1974. F. S. and Bradley D. J. Egg output stability 2. McCullough and the epidemiology of Schistosoma haematobium. Part 1. Variations and stability in Schistosoma haematobium egg counts. Trans. R. Sot. rrop. Med. Hyg. 67,475-490, 1973. and stability in 3. Wilkins H. A. and Scott A. Variation Schistosoma haematobium egg counts: a four-year study of Gambian children. Trans. R. Sot. trop. Med. Hyg. 72, 397-404, 1978. 4. Bradley D. J. Regulation of parasite population. Trans. R. Sot. trop. Med. Hyg. 66, 697-708, 1972. of helminth 5. Bradley D. J. and May R. M. Consequences aggregation for the dynamics of Schistosomiasis. Trans. R. Sot. trop. Med. Hyg, 72, 262, 1978. 6. Polderman A. M. The transmission of intestinal Schistosomiasis in Begemer province, Ethiopia. Thesis. Leiden, 1975. I. Polderman A. M. et al. Intestinal schistosomiasis in the mining district of Maniema. Kivu province. Zaire. Parts 1 and 2. Annls Sot. beige Med. trap. Accepted for publication. 8. Chesterman C. Note sur la bilharziose dans la region de Stanleyville (Congo Belge). Ann/s Sot. helge M&d. frop. 3, 73-76, 1923. 9. Fisher A. C. A study of the schistosomiasis of the
1080
10.
I I. 12. 13.
A. M. POLDERMAN
Stanleyville district of the Belgian Congo. Trans. R. Sot. trap. IVied. Hyg. Zg, 277-306. 1934. Berghe L. van den Les schtstosomes et les schistosomoses au Congo Belge et dans les territoires du RuandaUrundi. Institute Royal Colonial Beige, MemoiresCollection. 1939. Gillet J. and Wolfs J. Les bilharzioses humaines au Congo Belge et au Ruanda-Urundi. Bull. Wld Hlrh Org. 10,315-419, 1954. Schyns Ch. Personal communication. Polderman A. M., Kayiteshonga Mpamila, Manshande J. P.. Gerold J. L.. De Vries H. and Gryseels B. On the
distribution and control of schtstosomiasis mansom in Maniema. Zaire. Acta Leidensia 49. 17-29. I98 I. 14. Ee J. H. van and Polderman A. M. Physiologtcal performance and work capacity of tin mme labourers m Zaire infested with schistosomiasis. Twp. gqy. .Jfud. Accepted for publication. 15. Polderman A. M. and Manshande J. P. Futlure of targeted mass treatment to control schtstosomtasis. Lancer 3 January, 1981. 16. Epidemiology and control ofschistosomtasis. Report ofa WHO Expert Committee. WHO Technical Report Series No. 643.