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Human Schistosomiasis in India? V.R. Southgateand M.C. Agrawal It was a common belief in the first half of this century that human schistosomiasis would not become established in India, despite the regular introduction of the disease by soldiers returning from active campaigns. This was based on the absence ol known intermediate hosts for Schistosoma spp, yet in 1952 a focus of human schistosomiasis was discovered in Gimvi village, Ratnagiri District, Maharashtra State. The focus seems to be in recession, but the proposed large irrigation schemes centering upon the Narmada River may exacerbate schistosomiasis in domestic stock, and possibly in humans. Here, Vaughan Southgate and Matesh Agrawal discuss the findings in Gimvi, and the possibilities of human schistosomiasis in India in the future. India has had contact for centuries with countries such asJapan, China and Egypt, all of which have endemic human schistosomiasis (Schistosoma joponicum in Japan and China, S. mansoni and S. haematobium in Egypt). During the past century, wars have resulted in the movement of Indian troops to various African and Asian countries, it is not surprising that some troops, on returning to India, carried active schistosome infections. During this period none of the known intermediate host species was found in India, nor were any endemic snails found to be compatible with human schistosomes 1'2.In addition, it was a widely held view that S. hdematobium and S. mansoni developed only in humans, and other species developed solely in either wild animals or domestic stock. Later, laboratory and field studies have shown that such rigid definitive host specificity with regard to 'human' schistosomes does not exist. For example, both S. mansoni and S. japonicum have been shown to have a wide range of definitive hosts, and S. hoematobium is not restricted to humans 3. For the first half of this century the absence of known intermediate hosts of human schistosomiasis in India created a strong feeling within the scientific community there that human schistosomiasis would not become established in their country. However, in 1952 Gadgil and Shah4 reported a focus of human, urinary schistosomiasis in Gimvi village (Figs I and 2) Ratnagiri District, Maharashtra State, with 205 people passing S. haema-
tobium-shaped eggs in their urine. As some of the infected children had never previously left the area, all the evidence pointed towards an active transmission focus in Gimvi. There is a small rivulet passingthrough the village, in which several species of freshwater mollusc are found, including Indopldnorbis exustus, Lymnaea luteold, Paludomus obesa, Ferrissia tenuis and Melanoides tuberculata. Subsequently, numerous different species were exposed to miracidia originating from the patients, and the only species found to shed schistosome cercariae, despite heavy mortality, was the very small ancylid snail, F. tenuis (Fig. 3)5. tn an examination of 1200 F. tenuis, Sathe and Renapukar 6 found only 12 specimens to be infected with schistosome cercariae. On this evidence, it has been generally assumed that F. tenuis is responsible for transmission. This is somewhat surprising, since I. exustus and L. luteola are intermediate hosts for mammalian schistosomes, and, apart from this focus, S. haematobium is only known to be transmitted by snails belonging to the genus Bulinus. Compared to other known intermediate hosts of schistosomes, the cercarial productivity ofF. tenuis per snail is low, simply because of the small size of the snail. The low productivity is probably compensated for by massive snail
population densities (up to 200 specimens may be found on one leaf). Interestingly, snails of the genus Ferrissia are widely distributed throughout much of India and Africa, but have never been incriminated elsewhere in the epidemiology ofS. hoematobium, nor indeed in any other species of mammalian schistosome, tt must be remembered that host-parasite relationships are dynamic and continually evolving, and schistosomes with a wide geographic distribution, such as S. haematobium, exhibit intraspecific variation that may manifest itself in distinct differences in intermediate host specificity 3. That said, the restriction of the human focus of the S. haematobium-like infection to Gimvi remains enigmatic, and the epidemiology of the infection is difficult to understand. There have been sporadic reports of humans passing eggs in either faeces or urine in various parts of India, but in reviewing these reports, Anantaraman 7 concluded that some of them lack scientific basis and others are probably based on eggs of 'animal' schistosomes being passed by humans after the ingestion of infected animal tissues. Anantaraman 7 also pointed out that there are eight species of schistosome occurring in animals in India (S. incognitum, S. indicum, S. nasale, S. spindale, Orientobilharzia
Fig. I. Transmission site of human schistosomiasis, Gimvi, Maharashtra State. ~) 1990,Dsevler SciencePublishersLtd, (UK) 0169 4707/90/$02.00
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167 understanding of its taxonomic position within the S. haematobium group. Advances in the use of DNA probes have enabled workers to distinguish S. haematobium from its close relatives by a characteristic 0.5 Kb deletion in the nontranscribed spacer region of the rRNA gene 12. If material is still available, it would be very useful to establish whether or not the Gimvi schistosome has this characteristic deletion. The apparently limited distribution of the transmission focus of the human schistosome to Gimvi is in some ways fortuitous, in the light of the enormous irrigation scheme currently being constructed on the Narmada River, part of which forms the boundary between the States of Maharashtra and Gujarat. The Narmada Valley Development Project (NVDP) is one of the largest schemes of its kind in the world, and entails the construction of 30 major dams, 135 medium dams and 3 000 minor dams on the Narmada River and its tributaries in the next forty years (Fig. 4). Hydroelectric power will be generated from some of the major dams. It is recognized that the creation of the largest man-made lake in India and the resulting irrigation schemes will have an enormous environmental and ecological impact on the entire ecosystem. It seems likely that freshwater snails, including F. tenuis, L. luteola and I. exustus, intermediate hosts of human and veterinary schistosomiasis, will colonize at least parts of this new irrigation scheme. Indeed, the National Institute of Communicable Diseases has undertaken a project of risk assessment, examining urine samples of people from randomly selected villages falling within
Sardar~B~urdwa n f Fig. 2. Sketch map of India, showing the posit~on olr Gimvi, Maharashtra State; Dokur, Andhra Pradesh; Burdwan District, West Bengal and Sardar Sarovar in relation to Delhi and Bombay.
bomfordi, O. dattai, O. turkestanicum and Bivitellobilharzia nairi). In fact, S. incogniturn was first reported from two human faecal samples, but subsequently disputed as a blood-fluke, of humans8. Zoonotic aspects of this and other mammalian schistosomes are yet to be determined, leaving open the possibility of interspecific interaction and emergence of forms that may be infective to humans. Since the original report, the focus of human schistosomiasis at Gimvi has been confirmed by several different workers, including Dave and Dhage 9 and Oliver I°. More recently, Gaitonde. et al. i i found only four out of 607 urine specimens examined to be positive for schistosomes. Sathe (unpublished) believes that there are now no cases in Gimvi, which suggests that the infection may have been eradicated. Treatment of the positive cases by chemotherapy seems at least to have significantly reduced prevalence. Further monitoring will be necessary to confirm these observations. On reflection, there are many facets about the Gimvi focus that remain puzzling. Is the parasite responsible for the infection in humans S. haematobium? Certainly on the basis of size and shape of the egg and the location of the parasite in the definitive host, ie. the veins around the: bladder, the answer is yes. Unfortunately, the schistosome from Gimvi has never been isolated and established in the laboratory, and so has not been subjected to analyses using enzyme electrophoresis and DNA recombinant technology, which are ,essential for a more complete characterization and
o r~
Fig. 4. Early stages of the construction of the dam at Sardar Sarovar, Narmada River.
the submergence area. Clearly, it will be prudent to maintain a programme of monitoring, so that any introduction of human schistosomiasis can be dealt with effectively. The possibility of additional foci of human schistosomiasis elsewhere in India exists. For example, there have been at least two reports of schistosome eggs appearing in urine and/or faecal samples in India in 1989. Bidinger and Crompton 13 report the finding of terminal-spined schistosome eggs from two stool and two urine samples originating in the environs of Dokur, Andhra Pradesh (Fig. 2). These authors do not comment upon the viability or dimensions of the ova, but recognize the need for further studies to establish the identity of this putative schistosome. In addition, Anuradha et al. 14 reported a case of hepatic schistosomiasis in a patient from Burdwan District, West Bengal (Fig. 2), where the eggs passed were typical of S. mansoni. As yet, there is no additional evidence of transmission foci of human schistosomiasis in either Dokur or Burdwan District, but further field studies are desirable to clarify whether these cases represent active infections or contamination. Looking to the future, international scientific collaboration should help to elucidate some of the long-standing and relatively poorly understood problems of endemic schistosomiasis on the Indian subcontinent. Acknowledgements
Fig. 3. Shell of the ancylid snail,. Ferrissia sp. Scale bar = 2 ram.
We thank D.S. Brown and D. Rollinson for their constructive comments, B.D. Sathe for
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help in the field and the Parasitic Diseases Programme, WHO, for financial support. References
I Baugh, S.C. (1978) Revta Iber, Parasitol. 38, 435-472 2 Chauhan, O.S. and Chauhan, Y.S. (1957) in Dr Sir Hari Gour Commem. Vol, pp 296-306, University of Saugur, India 3 Rollinson, D. and Southgate, V.R. (I 987) in The Biology of Schistosomes: from Genes to Latrines (Rollinson, D. and Simpson, A.J.G., eds), pp 1-49, Academic Press 4 Gadgil, R.K. and Shah, S.N. (I 952) Indian]./Vled. Sci. 6,760-763
5 Gadgil, R.K. and Shah, S.N. (I 955) Indian]. Med. Res.43, 695-70 I 6 Sathe, B.D. and Renapukar, D.M. (1983) Bul. Haffkine Inst. I I, 8 7 Anantaraman, M. (1984) Indian Geog. J. 59, 13-17 8 Agrawal, M.C. and Shah, H.L. (1989) Helm. Abs. 58,239-25 I 9 Dave, P.J.and Dhage, K.R. (I 958) IndianJ. Med. Res. 46,546-556 I 0 Oliver, LJ. ( 1961) WHO Tech. Rep. No. I 19 II Gaitonde, B.B. et al. (1981)Indian]. Meal Res. 74, 352-357 12 Rollinson, D., Walker, T.K. and Simpson, A.J.G. (1986) Parasitology Today 2, 24-25
13 Bidinger, P.D. and Crompton, D.W.T. (1989) Trans. R. Soc. Trop. Meal. Hyg. 83,526 14 Anuradha, S., Panigrahi, H.C. and Nagalotimath, S.J. (1989) The Indian Pract. XLII, 297-299
Vaughan Southgate is at the Department of Zoology, The Natural History Museum, Cromwell Road, South Kensington, London SW7 5BD, UK, and Nlatesh Agrawal is at the Department of Parasitology, College of Veterinary Science and Animal Husbandry, Jabalpur, MP 48200 I, India.
Bee s The Origins of Human
Disease by ThomasMcKeown, BasilBlackwell, 1988. £39.50 hbk, £ 14.95 pbk (vi + 233 pages) ISBN 0 631 15505 8 This is a thought-provoking book. A recurring theme is that the overall improvement in health of humans over the centuries has been largely due to improved nutrition, but it is also known that stress promotes disease. Hence, epidemics of plague followed years of famine in Europe and elsewhere, and outbreaks of louse-borne typhus followed the turmoil of war. However, the non-communicable diseases, which the author calls 'the diseases of affluence', are also the result of the stresses of modern society. There is also the evolutionary theme of human huntergatherer communities, exposed to zoonotic infections and to commensal parasites, developing into expanding agricultural societies, where human-tohuman transmission without an animal reservoir became important, and where, the author believes, food deficiency was a major determinant of disease. Then during the nineteenth century the industrial revolution in the developed world led to a rapid rise in population coinciding with the development of modern medical practice. Over this period, human genes were selected for survival in varied environments very different from those of today's more affluent societies. The author questions the view of primitive man being in harmony with his environment, since if this was so, why was life expectancy so short? Why did about seven out of every ten people born before the eighteenth century die before maturity? Why was respiratory tuberculosis in decline in England and
Wales before the discovery of the tubercle bacillus in 1882? Furthermore, this decline continued until the development of effective treatment by streptomycin in 1947 and immunization by BCG vaccine in 1954. Most of the decline (57%) took place before 1900 and although modern treatment halved the death rate, modern therapy only contributed a reduction of 3.2% to the general trend. This raises the question of which is the more important in the control of parasitic disease today in the developing world, chemotherapy, vector control, improved sanitation, or changing human behaviour? One conclusion is that the Third World is essentially unchanged from early times and although sufficient food is available to feed it, it is unequall~rdistributed. Drinking water and sanitation are grossly defective and the difficulties are compounded by rapid population growth, plus an increase during the present century of conditions such as diabetes, hypertension and obesity, that divert medical care. Parasites could be regarded as diseases of human poverty. One heard in the 1960s that all the communicable diseases could be controlled worldwide in the forseeable future but we have seen the return of malaria. The Public
The Macmillan Dictionary of Immunology byF.S. Rosen,LA. Steinerand E.R. Unanue, The Macmillan Press, 1989. £25.00 hbk, £9.95 pbk (vii + 223 pages) ISBN 0 333 39248 5 Immunology is nothing if not riddled with jargon, and I found the original Dictionary of Immunology produced by Blackwell
Health Laboratory Service in the UK was facing contraction until the arrival of AIDS. The International Drinking Water Supply and Sanitation Decade of the United Nations is almost over. In 1983, three out of four urban residents had access to a safe water supply and a little over half had access to adequate sanitation, and two out of five rural dwellers had access to a safe water supply and one out of seven to appropriate sanitation. Can this rate of change be sustained at a time of crippling debt in the Third World? There are conclusions in this book but no obvious solutions. 'The poor are always exposed to the worst of prevailing conditions and it is even more obvious today'. It ends with, 'We cannot respect the judgement of people who are so preoccupied with the present that they give no thought to what is to follow', but we cannot trust the motives of those who can ignore existing problems when designing a future blueprint.' One could add that, with the late Professor PlcKeown, we should look to the past in tryingto see into the future. B.EL Laurence
School of Biological Sciences University of East Anglia Norwich Norfolk NR4 7TJ, UK
(now in its third edition by w.J. Herbert, P.C. Wilkinson and D.I. Stott)invaluable in my formative years. This is now joined by a competitor, the subject of this review, and the two must attract comparison. The new book has a different approach to its predecessor in that it has a smaller vocabulary but it goes in for long, quite detailed entries, which are informative, but might be intimidating to some newcomers. On the other hand, the depths that immunology has now