Nutritional aspects of infection

TRANSACTIONS OFTHEROYALSOCIETY OFTROPICAL MEDICINE ANDHYGIENE (1986)80, 697-705

Nutritional

aspects

697

of infection

D. W. T. CROMPTON Dept. of Zoology,

University

of Glasgow, Glasgow G12 8QQ, Scotland

Abstract Current knowledge is examined about the means whereby ascariasis, hookworm disease, strongyloidiasis and trichuriasis may contribute to the aetiology of human malnutrition. Results from experiments with related parasites in the laboratory have demonstrated the role of gastrointestinal helminthiases in animal malnutrition. Some evidence shows that in children, infection with the intestinal stages of Ascaris lumbricoidesis associatedwith reduced growth rate? disturbed nitrogen balance, malabsorption of vitamin A, abnormal fat digestion, lactose maldigestlon and an increased intestinal transit time. The main impact of hookworm infection is its relationship with iron-deficiency anaemia which may have effects at the community level as regards work and productivity in adults and learning and school performance in children. More researchis needed to extend knowledge of the nutritional impact of ascariasis and hookworm disease in order to establish their public health significance. Researchis needed also to identify the range of nutritional effects on man that occur as a result of trichuriasis and strongyloidiasis. The significance of less prevalent and more localized gastrointestinal helminthiases should not be ignored. Introduction Roughly half of the world’s population lives under the conditions that generate nutritional stress and parasitic disease.Protein-energy malnutrition (PEM), which impairs the growth and development of children, is probably the world’s major public health problem with iron-deficiency anaemia and vitamin A deficiency being other outstanding afflictions (CROMPTON & NESHEIM, 1982, 1984; LATHAM, 1984). Inadequate production or shortage of food are no longer thouiht to be the usual causesof malnutrition (LATHAM. 1984‘1;instead the nroblem develoos from &d is m&n&id by a complex network o’f socioeconomic determinants (CRAVIOTO& DELICARDIE, 1976; WOOD & CALLOWAY,1984). Malnutrition and parasitic diseasehave a strikingly similar geographical distribution with the same people experiencing both insults together for much of their lives. Gastrointestinal hehninthiases flourish where poverty prevails, where sanitation is inadequate or non-existent and where more health awareness and care are needed (WHO 1981). Gastrointestinal hehninths live in probably the most influential site of the body with regard to the host’s nutritional health and status. In the light of the experience gained in concluding that malnutrition usually arises from a more complex aetiology than food shortage, it would be naive to suggest that gastrointestinal helminths cause malnutrition. Current knowledge does permit us, however, to ask two important questions. First, do gastrointestinal helminthiases contribute to malnutrition? Secondly, if it be shown that these helminths are implicated in the aetiology of human malnutrition, what action should be taken to relieve man of this particular stress? Action aimed at the control of gastrointestinal helminthiases will depend on community programmes founded on recent epidemiological research; inevitably this effort will require technical and administrative skil!, .equipment, drugs and financial sunwrt. The declslon to establish a control programme will probably depend on an

evaluation of the net benefits, bearing in mind that the implementation of the control will compete with the needs of other health issues (PRESCOTT& JANCLOES, 1984). The maximum benefit with the minimum risk must be achieved for the people involved (HABICHT, 1985).

It is, therefore, imperative that the public health significance of gastrointestinal hehninthiases should be established accurately; this will depend on more field research aimed at the measurement of morbidity and mortality rates. The hypothesis under test is that the major component of the morbidity of gastrointestinal helminthiases is a chronic and insidious contribution to human malnutrition. Parasitism and nutrition Gastrointestinal helminths are arbitrarily defined here as the species of parasitic worms living for an obligatory period in the human gut or its associated ducts. Thus Fasciola hepatica would qualify because the adults occupy the biliary system while Schistosoma mansoni living in the hepatic portal system would not, although its habitat is undoubtedly linked to its host’s nutritional physiology. According to MULLER (1975), about 100 species of helminth have been reported from the human alimentary tract. Of these, the nematodesAscaris lumbricoides, hookworms (Ancylostoma duodenale and Necator americanus) and Trichuris trichiura are the most common with prevalence values of about 1000, 900 and 500 million cases per year, respectively (PAWLOWSKI, 1984a). The nematode Strongyloides stercoralis is another potentially important gastrointestinal hehninths as regards human nutrition (WHO 1981), but its prevalence is much less than that of the four species of soil-transmitted helminths named above (PETERS& GILLES, 1977). The diseasesassociatedwith the major soil-transmit: ted helminths have become known in developed countries as the neglected diseases (BRUER, 1982). This apparent neglect is hardly surprising when a volume of 621 pages, published in 1977 with the title

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SYMPOSIUM-GASTROINTESTINAL

A Wortif Geography of Human Diseases, contained no obvious mention of Ascaris lumbricoides and T. trichiura while hookworm is referred to in one

sentence on page Il. This review has been restricted to a brief discussion of ascariasis, hookworm disease, strongyloidiasis and trichuriasis. Other gastrointestinal hehninthiases may be extremely important in a particular country or region. Fasciolopsis buski is associatedwith nutritional diseasein S.E. Asia and the Far East (CROSS,1969), Capillaria philippinensis remains a nuiritionai threat after its acute outbreak in the Philinnines in 1967 (WHALEN et al., 1969; FRESHet aL.,‘*1972), Hymerwlepis nana may be involved in disease(PAWLOWSKI, 1984b) and Diphyllobothrium latum is known to cause in certain p&nts a syndrome remarkably like nernicious anaemia &ON BONDSDORFF, 1977). iir’chinelka spiralis is a c&se of nutritional disturbande in animal hosts (CASTRO & OLSON, 1967), but apparently not in man (GOULD, 1970) apart from diarrhoea soon after the establishment of infection (KAZURA, 1984). Nutrition in man seems to involve economic, political, cultural and psychological factors which $teract -and influence thh supply-and distribution of food within the communitv and familv (WOOD & CALLOWAY,1984). Individial food in&e ‘in healthy animals, and probably in people, is under neural and hormonal control and is thought to be a response to satisfy an energy deficit (MORGENSON8z CALARESU, 1978). This process results in the intake of most nutrients in the appropriate amounts given that the food is varied and of adequate quality. Nutrients amount to about 45 elementsand cGmpo&ds (SCRIMSHAW& YOUNG. 19761and are those items of food that may or may hot be’releasedduring digestion, but must be absorbed from the gut and utilized in the tissues. The food contains other non-nutrient items such as roughage or dietary carbohydrate which also contribute to the health and well-being of the individual (DAVIDSON et al., 1975). Nutrients are required in quite precise amounts (WOOD & CALLOWAY, 1984) which change according to the age and physiological needs of the person concerned. An infected person must obtain and supply, usually indirectly rather than in the form of the food itself, all the nutrients required by the parasite during its period of obligatory dependence. Even a seeminglv huge worm curden, for example 1000 adult x. lumbricoides. will form onlv a small fraction of the biomassof ihe infected host’and direct food robbery is not likely to be of much nutritional significance (VON BRAND, 1973). If the host is feeding on an inadequate diet, however, any loss to an infection must make some small c&tri6ution to malnutrition. FORSUMet al. (1981) found that A. suum in Digs fed on a diet co&in&g a normal amount of proie& weighed more than worms from pigs fed on a low protein diet. Much experimental evidence from work with laboratory rodents infected with natural parasites shows that the growth, longevity., fecundity and asexual reproduction of hehninths 1ssensitive to changesin the quality and quantity of the host’s dietary intake (CROMPTON, 1986). Another nutritional interaction between hosts and their gastrointestinal helminths is the exploitation by the parasites of the feeding behaviour and food of their hosts to facilitate and ensure transmission and survival.

HELMINTH

INFECTIONS

Evidence

from animal experiments

The results from any investigations of the course of primary infections of naturally occurring host-parasite relationships maintained under controlled conditions in the laboratory have established unequivocally that host nutrition in all its forms is adverselv affected bv the presence of parasitic helminths (NE~HEIM, 1984, 1985). Food intake is reduced (SYKES& COOP.1977: SYKES, 1982; CROMPTON, 1$84; SYMONS, 1985); growth rate is retarded (SYKES & COOP, 1977), maldigestion and malabsorption occur (SYMONS, 1976; CASTRO, 1981) and metabolism is disturbed (ASHet al., 1985a,b; OVINGTON,1985). The fact that pair-fed uninfected hosts grow better than their infected partners points to the more efficient use of nutrients-in the absence of infection (CROMPTONet al.. 1981). Laboratorv exDeriments differ in manv ways from natural inf&tio& where recruitment a&l loss of parasites occur, environmental stressesexist and interactions take place between infections. However, experiments identify possible effects and greatly improve the chances of detecting causation. Recent experimental results of particular significance to the theme of this review concern studies with Ancylostoma tubaeforme and A. ceylanicum in cats and dogs (ONWULIRI et aE., 1981; CARROLLet al., 1984; lk5j, Ascaris suum inpigs (STEPHENSON et al.; 1980a:FORSUMet al.. 1981: BAKKER. 1984: MARTIN et al.,‘ 1984), Strongy~oides ransomi in’pigs (ENIGK & DEY-HAZRA, 1975)and Trichuris suis in pigs (BECK& BEVERLEY-BURTON, 1968; HALE & STEWART,1979). These studies demonstrate how host nutritional status is impaired by parasitesthat are closely related in their biology to those that make up the assemblageof major gastrointestinal hehninths in man. Gastrointestinal

helminthiases

in man

The impact of gastrointestinal hehninth infections on human-nutrition has been reviewed by SOLOMONS 8~ KEUSCH (1981) and ROSENBERG& BOWMAN (1984). The ‘evid&ce that can be interpreted as showing that nutritional impairment accompanies gastrointestinal helminthiases is obtained from clinical investigations with relatively few, specially selected patients, and from community studies where control is difficult to achieve, where polyparasitism is a confounding variable and where-id&l study designs (SCHULTZ,1982; STEPHENSON.1984: CROMPTON& STEPHENSON, 1985) cannot usially be implemented. The approach to the assessmentof nutritional status has been outlined by WOOD & CALLOWAY(1984). Ascariasis

The presence of the adult stagesof A. lumbricoides in the human small intestine is associated with impaired nitrogen balance as detected by excessive faecal nitrogen loss in infected children (VENKATACHALAM & PATWARDHAN, 1953), accelerated mouth to caecum transit time (TAREN et al., 1986), malabsorption with typical villus atrophy (TRIPATHY et al., 1971, 1972), lactose maldigestion (CARRERAet al., 1984; TARENet al., 1986)and reduced absorption of vitamin A (SIVAKUMAR& REDDY, 1975; MAHALANABIS et al., 1976, 1979). Although causation is difficult to demonstrate in people, some studies revealed remission of the lesion following anthelmintic treatment (TRIPATHY et al., 1972; TAREN et al.,

D.

W.

T.

1986) and a relationship between the severity of the lesions and the intensity of infection (CARRERAet al., 1984). A relationship between the intensity of infection and the degree of nitrogen and fat absorption was found by BROWNet al. (1980) who observed statistically significant improvements in the absorption of these macro-nutrients by children given anthehnintic treatment to remove heavy infections. The malabsorption detected during ascariasis, or other gastrointestinal helminthiases, is not easily explained or investigated because over 50 conditions are known during which chronic malabsorption may arise (BANWELL, 1984). CARRERAet al. (1984) and TAREN et al. (1986) showed that lactose digestion, commonly associatedwith malabsorption (BANXVELL, 1984), was diminished during ascariasis. Parallel experiments with pigs infected with A. suum showed that mucosal lactase activity was significantly reduced and that the architecture of the microvillus brush border of the intestinal epithelium had been disturbed. However, electron micrographs suggested that the presence of A. suum might have altered the small intestine in favour of bacterial colonization (MARTIN et al., 1984). Earlier TOMKINS et al. (1978) proposed that intestinal colonization by enterobacteria in patients with Giardia intestinalis might contribute to the development of malabsorption during giardiasis. On a community basis, the interpretation of anthropometric measurementsagainst internationally agreed standards (JELLIFFEE, 1966; WOOD & CALLOWAY, 1984) is frequently used to assessnutritional status with the detection of degrees of PEM as the main objective of the surveys. Pre-school children are most vulnerable to PEM and usually many of those living in an endemic area for A. lumbricoideswill have acquired the parasite by the time they are five years old (ANDERSON,1985). Given the limitations of the study designs and the contraints imposed on field work by local conditions and attitudes (CROMPTON & STEPHENSON,1985), growth retardation related in some way to ascariasishas been detected in children from Deoria District, U.P., India (GUPTA et al., 1977), from Lushoto, Tanzania (WILLETT et al., 1979), from Machakos District, Kenya (STEPHENSON er al., 1980b), from Bali (CERFet al., 1981) and from Kuala Lumpur, Malaysia (KAN et al., 1983). Importantly, CERF et al. (1981) found that the effect of ascariasis on nutritional status was conditional on socio-economic status. This finding and the fact that the frequency distribution of numbers of A. lumbricoidesper person is overdispersed (ANDERSON,1985) must be accommodated in the data analysis. In addition to the studies cited, the results of several others point to the possibility of an association between ascariasis and- childhood malnutrition. As with the more phvsiologicallv orientated studies. the mechanisms underlying growth retardation are not yet understood, but it is tempting to suggest, because of the convincing results from pig-A. suum studies (FORSUMet al., 1981), that reduction in food intake will be an important factor. Measurement of food intake for people living in their normal environment is extremely difficult co achieve (SANJUR,1982; WOOD & CALLOWAY.1984). esneciallv if the observers are from a differ&t culture: In a recent study in Panama, which included an attempt to assessthe

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effect of ascariasison milk consumption as measured by lactose intake, the 24 hour-recall method detected that infected children took significantly less lactose than uninfected children while food weighing did not reveal the difference (NESHEIM et al., 1985). The study in Panama also obtained new epidemiological evidence to support the clinical finding that ascariasis may contribute to vitamin A deficiency (SIVAKUMAR & REDDY, 1975; MAHALANABISer al., 1976, 1979). Plasma vitamin A concentration in 56 Ascaris-infected children was found on averageto be 30-O+ 1.0 ug/dl, a value sienificantlv less (P
nuslive attached by their mouthparts to the mucosa of the small intestine where their feeding activity, now known to be facilitated in the caseof A. duodenale by the secretion of a proteolytic enzyme with anticoagulant activitv (HOTEZ & CERAMI. 1983). leads to a loss of host blood (ROCHE81 LAY~ISS&“~~~~). Widely accepted estimates, based on a variety of radioisotopic studies, suggest that from O-14to 0.26 ml of faecal blood is lost per day due to one A. duodenale and 0.02 to O-07 due to one N. americanus (LAYRISSE et al., 1976). Iron-deficiency anaemia is regularly associatedwith hookworm disease (BORREROet al., 1961; ROCHE& LAYRISSE,1966; MASUYA, 1980), with the anaemia being defined as the condition resulting from the inability of the erythropoietic tissue to maintain a normal blood haemoglobin concentration (LAYRISSEet al., 1976). Normal haemoglobin concentrations differ dewnding on the age and sex of the subjects, pregnancy and lactation and altitude (WHO. 1972). Estimation of blood haemoglobin concentration is the most straightforward measurement to make in a community in regions where hookworms are prevalent (LATHAM, 1984), but the results give no indication of the state of the body’s iron stores which will be running down as the body strives to maintain blood haemoglobin

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HELMINTH

INFECTIONS

concentration (WEATHERALL 81 WASI, 1984). Irondeficiency anaemia can be more comprehensively studied by measuring serum ferritin and serum iron concentrations and the percentage of transferrin saturation at the same time as blood haemoglobin concentration is measured. MANSOURet al. (1985) used this protocol in an investigation of iron deficiency in 103 adult male patients with chronic schistosomiasis mansoni. 52 (~50%) of the subjects had blood haemoglobin values below 13g/lOOml,a value taken to be normal. Of the remaining 51 subjects, 42 were judged to have latent iron deficiency on the basis of serum ferritin concentrations and 16 had abnormal values for percentagetransferrin saturation. This type of study might provide much useful information about iron-deficiency anemia during hookworm infection. The iron status of the body can be maintained by the daily absorption from the small intestine of iron varying from 0.7 mg (infants, 5 to 12 months) to 3 mg (women, second half of pregnancy) (WHO, 1975). The availability of iron depends on daily intake, the body’s needs, whether the iron is obtained from vegetablesor meat, the ratio of vegetable iron to meat iron, dietary factors that enhance and inhibit iron absorption and the condition of the intestinal absorptive surface (LYNCH, 1984; WEATHERALL& WASI, 1984). The balance that develops between dietary iron intake, bioavailability and absorption is affected by chronic iron losses such as menstruation. According to WEATHERALL& WASI 0984) chronic blood loss from the gastrointestinal tract of from 15 to 20 ml will produce a negative iron balance despite an increase in iron absorption and reabsorption. They also state “in tropical populations, hookworm infection is by far the commonest causeof gastrointestinal blood loss”. It is perhaps unwise to attempt to calculate the number of hookworms that can cause losses of the magnitude cited by WEATHERALL & WASI (1984), but even conservative estimates point to a strong impact of hookworm infection on human nutrition. CLINE et al. (1984) described the signs and symptoms of hookworm diseasein 21 patients infected with N. americanus. 14 patients were positive for at least one of six gastrointestinal symptoms (abdominal pain, diarrhoea, nausea, vomiting, belching and flatulence) someof which would be associatedwith a reduction in appetite. In some cases the course of a hookworm infection has been accompanied by villous atrophy, steatorrhoeaand malabsorption (SHEEHY et al., 1962). A survey in Papua New Guinea found a relationship between poorer nutritional status and increasing intensity of hookworm infection (probably N. umericunus) based on weight for age and faecal egg counts reswctivelv (SHIELD et al.. 1981). Significant as these ex&ples of-impaired nutritional status may be, it seems unlikely that they will have the same general public health significance as the hookworms’ contribution to iron-deficiency anaemia.

1972) or either a new speciesor form of S. fkelleborni known for the nresent asS. cf. fuelleborni from Panua New Guinea (ASHFORDet al:, 1981). The unihue form of the ‘adaptable life-cycle centred on the activities of the larvae (GROVE. 1984) also contributes to the observed form‘of disease. ’ Acute strongyloidiasis due to S. stercorulis usually develops in adults in endemic areas with a massive build up of the tiny adult worms and larvae in the intestinal mucosa. The symptoms include diarrhoea alternating with constipation, weight loss, anorexia and vomiting (ONILE et al., 1985)and inevitably such a patient would be experiencing severe nutritional stress. Chronic strongyloidiasis, also due to S. stercorulis, seemsto occur in adults who have left an endemic area, perhaps for more than 30 years (GROVE, 1980). This continuation of the infection is explained by the autoinfection process as the larvae escape from the eggs while still in the alimentary tract. Out of 160 ex-service men, Grove obtained 44 who were infected with S. stercorulis and quantified their symptoms which, as far as nutritional interest is concerned, included diarrhoea in 20 of the 44 cases?indigestion m 32, weight loss in 10, abdominal pain m 25, anorexia in 11, nausea in 10 and lack of energy in 21 of the cases.He concluded that the worm had causedmuch ill health in many men for many years. Earlier O’BRIEN (1975) investigated in London seven former infantry soldiers who had been on active service in Borneo durine 1962 and 1963. Six of the seven patients presected with diarrhoea which began later in the seventh. Faecal fat excretion was elevated in the patients, D-xylose and vitamin Btr absorption were generally depressed and biopsy specimens showed partial villous atrophy in somecases.After anthelmintic treatment to expel the worms, the typical pattern of malabsorption was lost. The malabsorption syndrome so often described as a feature of chronic strongyloidiasis (ROSENBERG et al., 1977) is usually accepted on the basis of case reports or relatively small scaleclinical studies such as those described above or the investigation of MILNER et al. (1965) with four patients. Many hosts infected with S. stercorulis appear asymptomatic and KOTCHER et al. (1966) found no evidence of malabsorption during chronic strongyloidiasis and GARCIA et al. (1977) could not demonstrate malabsorption in patients harbouring S. stercorulis unless they were already malnourished. Chronic strongyloidiasis warrants detailed investigation of its possible interference in human nutrition at the community rather than clinical level. Occasionally, and apparently in immunocompromised hosts resulting from either therapy or possibly from concomitant infections or severe malnutrition, the larvae of S. stercorulis released in the intestine invade the tissues and lungs, usually with fatal consequences (GENTA et al., 1983). The disease causedby S. fwlleborni is virtually unknown, but may on the basis of one case history (PAMPIGLIONE &

strongy10idiusis

RICCIARDI,

Strongyloidiasis occurs in various forms depending on the age and geographical location of the hosts and whether the parasite involved is Strongyloides stercorulis, which has a worldwide distribution (FILHO, 1978), S. fuelkbomi, which is known from tropical Africa and parts of Asia (PAMPIGLIONE & RICCIARDI,

1972)

be similar

td the chronic

form

associated with S. stercoralis. The form of strongyloidiasis caused by S. cf. fwllebomi is known-as swollen belly syndrome and involves diarrhoea and the development of oedema in babies in Papua New Guinea (VINCE et al., 1979). The condition is not infrequently fatal and may perhaps be caused by a

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protein-losing enteropathy of the type suggested by LUNN (1981) to be of potential importance. Trichuriasis

Considering its high estimated prevalence and wide distribution. ielativelv little research has been done at the community levei on the pathology of Trichuris rrichiuru infection. The morbidity associated with trichuriasis is related to the adult worms and their mode of attachment to the wall of the large intestine (BECK 81 BEVERLEY-BURTON, 1968; PAWLOWSKI,

1984~).Rectal prolapse is the most spectacular lesion. Details of events with nutritional consequences during clinical trichuriasis in children can be abstracted from relativelv recent work bv MCKAY et al. (1971), KAMATH (1973), IYNGKARA~~ et al. (1976),

LEE et al. (1976), GILMAN et al. (1976), SCRAGG& PROCTOR(1977, 1978) and BOWIEet al. (1978) (see also BUNDY, 1986). Of the symptoms reported, diarrhoea, anaemia and hypoalbuminaemia are of concern. Chronic diarrhoea indicates malfunctioning of the gastrointestinal tract with a net loss of electrolytes and water if not nutrients. Severetrichuriasis has been associatedwith iron-deficiency anaemia and the feeding activity of the adult worms is reckoned to causea faecal blood loss from the host of about 0.005 ml per worm per day (LAYRISSEet al., 1976). Trichuris trichiuru is frequently found to occur concurrently with hookworms (ANNAN et al., 1986) and attempts to estimate its contribution to the aetiology of iron-deficiency anaemia will be difficult; iron lost into the large intestine may not be as readily available for reabsorption as that lost into the small intestine. Surveys making anthropometric assessments have shown that malnutrition may be present in children with trichuriasis (SCRAGG& PROCTOR, 1977). The possible relationship between these conditions needs to be examined in more detail as has been done for childhood malnutrition and ascariasis. Nutrition-mediated effects at the community level PRESCOTT& JANCLOES(1984) have drawn attention to issues that must be evaluated in the formulation of helminth control programmes. One simple question is “what will control cost?” and another is “will the expenditure on control be worthwhile?” or “will it be cost effective?“. Estimates of the costs of not having a control programme for a major parasitic disease like ascariasis or hookworm disease are difficult because little information is available in an appropriate form. Some tentative indications can be made for the nutrition-mediated effects of hookworm diseaseon communities provided that it is accepted that hookworm infections contribute to iron-deficiency anaemia. The first feature of the assessmentis to choose a suitable effect to investigate. In Ghana, 1482 healthy days of life were estimated as lost per 1000population due to hookworm disease (GHAPT, 1981), ranking hookworm infection as 36th in the list of 55 diseases studied. Usually, anaemia is associatedwith a diminished capacity to carry out physical work (LYNCH, 1984). Most people who suffer from hookworm anaemia live in a rural setting (95% of the population of Tanzania, according to KIHAMIA, 1981) where sustained periods of hard, labour-intensive physical work are essential to produce food for family survival

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and to maintain national agriculture and development. Several studies have identified the insidious effect of anaemia, in areas where hookworm prevalence is high, on work and productivity by investigating agricultural workers, construction workers, industrial workers and roadworkers in Indonesia, Kenya, Guatemalaand Tanzania (KARYADI & BASTA, 1973; DAVIES, 1973; DAVIES et al., 1973; VITERI & TORUN, 1974; SPURRet al., 1977; BASTA et al., 1979; BRINKS et al:, 1979; WOLGEMUTHet al., 1982). Direct causation by hookworm infection for the deleterious effects of the anaemia is not established, but the implication is there. WOLGEMUTH et al. (1982) showed that a difference of one standard deviation from the mean blood haemoglobin concentration was associatedwith a change of 5.6% in the productivity of road workers in Nyeri District, Kenya. BASTAet al. (1979) found that anaemic rubber tappers in an Indonesian plantation had on average 20% lessproductivity than non-anaemic counterparts. How would the costs of targetted treatment for hookworm anaemia in an area of high prevalence appear when compared with predictions for increased productivity? A rather subtle consequenceof hookworm anaemia, which may be even more difficult to quantify economically than effects on work output, concerns intellectual performance. Perhaps improvement in I.Q. might lead to measurable improvements in labour productivity as was proposed by SELOWSKY & TAYLOR (1973) after a study in Chile. Anaemic children, regardless of the presence of hookworm or not, are described as irritable., listless, apathetic and fatigued; none of these adjectives would normally be used for attitudes that promote learning and a lively school performance. Some 50 years ago, WILLIE & SPENCER (1926) considered that Necutor americanus hindered the school performance of children in Alabama where I.Q. scores decreasedas intensity of infection increased. Very recently, POLLITT er al. (1985), working with children in Java and Egypt, have found that non-anaemic children tended to be faster and more accuratewhen responding to standard tests than anaemicchildren, who responded positively later when given iron therapy. Conclusions The evidence shows that ascariasisand hookworm disease are known, under certain circumstances and in a variety of places, to contribute to malnutrition; ascariasisseemsparticularly to affect young children. Further research needs to be carried out to determine more quantitatively the public health significance of these gastrointestinal helminthiases. A smaller body of evidence suggeststhat strongyloidiasis and trichuriasis also contribute to malnutrition, but again more research is needed first to identify the range of effects and then to assesstheir public health significance. Other gastrointestinal helminthiases, which do not have the enormous prevalence of A. lumbricoides or hookworms, should not be ignored becausethey may have a more localized or regional impact. Researchand planning should also begin for efforts to implement programmes for the prevention and control of gastrointestinal helminthiases (PAWLOWSKI, 1983).

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Acknowledgements It is a uleasure to thank Dr. Z. S. Pawloswki of the Parasitic biseases Programme, WHO, Geneva, for many discussions and for his help with the literature for this review. I am also grateful to Mr. M. L. N. Murthy for editing and preparing the typescript. References Anderson, R. M. (1985). Mathematical models in the study of the epidemiology and control of ascariasisin man. In: Ascariasis and its Public Health Significance. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S. (editors). London & Philadelphia: Taylor & Francis, pp. 39-67. Annan, A., Crompton, D. W. T., Walters, D. E. & Arnold, S. E. (1986). An investigation of the prevalence of intestinal parasites in pre-school children in Ghana. Parasitology, 99, 209-217. Ash, C. P. J., Crompton, D. W. T. & Lunn, P. G. (1985a). Impact of Nippostrongylus brasiliensis (Nematoda) on the serum albumin and amino acid concentrations of rats fed adequate or protein-deficient diets. Parasitology, 90, 157-168. Ash, C. P. J., Crompton, D. W. T. & Lunn, P. G. (1985b). Endocrine responses of protein-malnourished rats infected with Nippostrongylus brasiliensis (Nematoda). Parasitology, 91, 359-368. Ashford, R. W., Hall, A. J. & Babona, D. (1981). Distribution and abundance of intestinal hehninths in man in western Panua New Guinea with suecial reference to Strongyloides. &mals of Tropical Med&ine and Parasitology, 75, 269-279.

Bakker, 1. (19841. Long term effects of a deworming prob& ‘using flube;dazole and levamisole on thi proportion of condemned livers in slaughtered pigs. Tijdschrtft voor Diergeneeskunde, 109, 815-819. Banwell, J. G. (1984). Malabsorption syndromes. In: Tropical and Geographical Medicine. Warren, K. S. & Mahmoud, A. A. F. (editors). New York: McGraw-Hill Book Company, pp. 14-29. Basta, S. S., Soekirman, M. S., Karyadi, D. & Scrimshaw, N. S. (1979). Iron deficiency anaemia and the productivity of adult males in Indonesia. American Journal of Clinical

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32, 916-925.

Beck, J. W. K. & Beverley-Burton, M. (1968). The pathology of Trichuris, Capillaria and Trichinella infections. Helminrhological Abstracts, 37, l-26. Blumenthal, D. & Schultz, M. G. (1976). Effects of Ascaris infection on nutritional status in children. American 3ownal of Tropical Medicine and Hygiene, 25, 682-690. Borrero, J., Restrepo, A., Botero, D. & Latorre, G. (1961). Clinical and laboratory studies on hookworm diseasein Colombia. American Journal of Tropical Medicine and Hygiene, 10, 735-741. Bowie, M. D., Morison, A., Ireland! J. D. & Duys, P. J. (1978). Clubbing and whipworm mfestation. Archives of Diseases in Childhood, 53, 411-413. Brooks, R. M., Latham, M. C. & Crompton, D. W. T. (1979). The relationship of nutrition and health to worker productivity in Kenya. East African Medical 3ouwm1, 56, 413-421. Brown, K. H., Gilman, R. H., Khatun, M. & Ahmed, M. G. (1980). Absorption of macronutrients from a ricevegetable diet before and after treatment of ascariasisin children. American Journal of Clinical Num’tion, 33, 1975-1982. Bruer, J. (1982). The great neglected diseases.Rockefeller Foundation Illustrated, June 1982, pp, 26-28. Bundy, D. A. P. (1986). Epidemiolo@cal aspectsof Trichuris and tricburiasis in Caribbean communities. Transactions of the Royal Society of Tropical Medicine and Hygiene, 80,

706-718. Carrera, E., Nesheim, M. C. & Crompton, D. W. T. (1984). Lactose maldigestion in Ascuris-infected preschool children. AmericanJoumal of Clinical Num’tion, 39,255-264. Carroll, S. M., Howse, D. J. & Grove, D. I. (1984).

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