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Intestinal parasitic worms and the growth of children
TRANSACTIONS OF THE ROYAL SOCIETY OFTROPICAL MEDICINE AND HYGIENE (1993) 87, 241-242
241
Leading Article Intestinal
parasitic
worms
and the growth
of children
WHO Collaborating Centre for the Epidemiology of Intestinal Parasitic Infections, Department of Biolog_y, Andrew Hall Imperial College, Prince Consort Road, London, S W7 2BB, UK
The popular concept that the food stolen by intestinal worms is responsible for thin children provides an intuitively reasonableexplanation for a direct effect on growth even without considering other, and possibly more important, effects such as impaired digestion and absorption, loss of appetite, gut leakage, and the nutritional costs and physiological consequences of the body’s responses to parasitic infections (HALL, 1985; LUNN & NORTHROP-CLEWES, 1993). But whatever the mechanisms, given that hundreds of millions of children are infected with worms and that many are also wasted and stunted, 2 of the main questions of public health importance are: does periodic treatment of worms reverse any effects on growth and allow catch-up growth to occur? and will enough children benefit to make parasite control a worthwhile intervention to improve child health and growth? In the last few years several studies have shown a beneficial imnact on growth of treating intestinal narasites (GILMAN-et al., i983; STEPHENSENet al., i989; COOPERet al.. 1990: THEIN-HLAING et al.. 1991) but others have not (FR~IJ et al., 1979; GREENBERG et al., 1981; GUPTA & URRUTIA, 1982), and this apparent inconsistency has created some perplexity and ambivalence. There are several biological, nutritional and epidemiological reasons why studies which aim to examine the impact of treating intestinal parasites on the growth of children might not detect an effect. First, many infected children live in environments where they are exposed from birth not only to the infectious stagesof several speciesof intestinal parasites, but to a variety of bacterial and viral diseasesas a result of crowding, contaminated food and water, inadequate sanitation and poor personal hygiene. The nutritional status of such children will reflect not only previous episodes of acute infectious diseasesin addition to concurrent, chronic infections with parasitic worms or protozoa, it will also reflect the adequacy of the diet to support satisfactory rates of growth. The impact of intestinal worms in such circumstances, where each child may have a different historv of infections and diet. will be verv hard to identify in cross-sectional surveys, so prospective studies of growth after treatment are necessary. Second,whether studies are cross-sectionalorprospective. it is inadeauate to classifv children simnlv into 2 groups, infected-and uninfected, as the severity of disease will depend on the intensity of infection. For example, a child with 50 or more Ascaris lumbricoides is much more likely to be diseasedthan one with 5 worms. This important point, which is special to worms, means that infection is not the same as disease. The number of worms necessary for there to be morbidity-a state which is vague and difficult to define for most intestinal worms becauseof a lack of specific signs or symptomswill depend on the speciesof parasite and on factors such as the age,,health and nutritional status of the host. Followmg from this point, even if all children in a community are infected with a speciesof worm, epidemiological studies have consistently shown that the majority are liehtlv infected. This is because intestinal narasites are n&her evenly nor randomly distributed among hosts but tend to be aggregatedin a few heavily infected individuals so that it is not unusual to find 70% of worms in 20% or fewer people (ANDERSON& MAY, 1991). Although such people are in a minority, in communities where the prevalence of infection is high significant numbers are still likely to be heavily infected and may experi-
ence morbidity so that, on a global scale, many tens of millions may be diseased. The aggregation of worms in hosts means that, if an effect on health or growth is to be detected, it will be necessary to stratify subjects by the intensity of infection rather than simply considering them as being infected or uninfected. At the level of the individual, therefore, it is important to assessthe intensity of infection at the time of treatment, either by a faecal egg count or, better still,, by recovering worms after treatment, although this is often impractical. At the community level it is necessaryto appreciate that the relationship between the prevalence of infection and the mean worm burden, an estimate of the intensity of infection in a community, is non-linear. Data from studies around the world on A. lumbricoides, for example, have shown that the mean worm burden is generally low when the prevalence is below about 60%, but may vary greatly when the prevalence is greater than 60% (GUYATT et al., 1990). This means that prevalence is a relatively insensitive indicator of any potential nutritional problem due to intestinal worms and that it is possible to have what may be perceived to be a high prevalence while the averageworm burden is small. A small average worm burden in a community or age class will tend to indicate that few individuals are heavily infected and that few will benefit from treatment. A third important point when considering the impact of intestinal worms is that the duration of infection before treatment is likely to be an important determinant of any growth faltering: a long-standing heavy worm burden is more likely to have had an effect than an equivalent but recently acquired worm load. The life spansof the common intestinal nematodes of humans range from 1 to 4 years (ANDERSON& MAY, 1991) and as individual worms recovered after treatment show a wide rage in size, probably reflecting their ageand the period since infection (ELKINS & HASWELL-ELKINS,1989), hosts probably tend to be infected for long periods with slowly fluctuating numbers of worms. There is no simple technique currently available to quantify such a state without recovering the worms after drug treatment. Fourth, it is necessaryto appreciate what in fact catchup growth presumes: a growth deficit in the first place, an adequate diet after treatment, a sufficient period for catch-up growth to occur, and freedom from disease. The nutritional status of a child before treatment is obviously important because the impact of treating a child of nearlv normal weight and height for age. if all else is equal, i’s likely to bg smaller than if the” child is both stunted and wasted before treatment. It is also reasonable that, if a child is to show catch-up growth after treatment for worms, then the child’s diet must be nutritionallv adequate to support catch-up growth in the first place, and that the child should be free from serious illness which might also impair growth. Such conditions do not always occur after treating children in the settings in which intestinal worms are most common, and heavily infected children are often drawn in the first place from the most deprived and vulnerable sections of the communitv. Because intestinal worms do not seem to orovoke a fully protective immune response in humans (BEHNKE, 1990), reinfection can occur immediately after treatment, although it may take some months before heavy worm burdens are reacquired: a study in Bangladesh of reinfection with A. lumbricoides found that, although treating children every 6 months with an anthel-
242 mintic did not reduce the prevalence of infection, it did serve to reduce mean worm burdens (HALL et al., 1992). In circumstances where the transmission of worms is very intense, it may be necessaryto treat all children repeatedly if catch-up growth is to be detected, and in communities where reinfection is rapid and diets are poor it may take many months and several rounds of treatment for an effect to be observed. A study in Burma of treating children every 3 months for A. Zumbricoides infections found significant increments in height gain after 6 months but significant gains in weight among treated children were observed only after 24 months (THEINHLAING et al., 1991). Fifth, in many communities multiple parasitic infections are the rule rather than the exception, and not all drugs for treating intestinal worms are equally effective: for example pyrantel pamoate, levamisole and piperazine are not effective against Ttichuris trichiuru (WHO, 1990). A selective approach to treatment, although scientifically precise, may be unrealistic, particularly in terms of public health. There are drugs available such asmebendazole and albendazole which are effective treatments for several soecies of intestinal nematodes (WHO, 1990) and single-dosesof albendazole have also been shown to have some effect against Giardia duodenalis (see HALL & NAHAR, 1993), another intestinal parasite associatedwith growth faltering (FARTHINGet al., 1986). Finally, there are someimportant features of study design which need to be recognized. If the impact of treatment is to be dissociated from other influences on growth, then an untreated control group is required (STEPHENSON,1987), and the cases and controls, whether allocated individually or by communities, should be similar in terms of initial parasitic infections and nutritional status. If allocation is done on a community basis, such as by village, then the sample size of villages must also be adequate. Studies which have met these criteria have shown an effect of treatment (STEPHENSONet al., 1989; THEIN-HLAING et al., 1991), but they can pose a dilemma when heavily infected and malnourished children are detected: if such children are excluded from the study on ethical grounds it will introduce a bias against the detection of a beneficial effect. This dilemma, between scientific needs and ethical imperatives, means that ideal studies are difficult to do and will always be easy to criticize if controls are in any way inadequate, so that the null hypothesis that intestinal worms have no effect on the growth of children could be acceptedin studies which fail to show an effect. But most studies which have come to such a conclusion, and it would be invidious or contentious to cite them, can be criticized becausethey are scientifically flawed for one or many of the reasonsgiven above. Unfortunately, because of the enidemioloaical and ethical nroblems of undertaking scientifically falid research this can lead to a position in-which, the cynics may argue, studies showing no effect will be disregarded while onlv those which show an effect will be accepted. Althou h several studies have shown an impact on growth oPtreating intestinal parasitic infections much attention has focused on children less than 5 years old, as this agegroup is considered to be particularly vulnerable. Nevertheless, in many communities the majority of children aged between 5 and 15 years are not only infected with at least one species of worm but they also tend to harbour the heaviest burdens (BUNDY et al., 1992). For these reasons a large proportion of this age group, which has in the past been rather neglected in terms of health care, could benefit during childhood from periodic treatment for worms. There are now available safe, low cost, single dose drugs to treat parasitic worms (WHO, 1990), and the fact that many children
aged 5 to 15 years congregate daily in schools provides a situation and an existing infrastructure in which periodic treatments could be delivered and thereby make a significant contribution to child health. Acknowledgements I thank Don Bundv. Kate Nokes and Fiona Watson for heluful discussions.
’’
References Anderson, R. M. & May, R. M. (1991). Infectious Disease ofHumans, Dynamics and Control. Oxford: Oxford University Press. Behnke, J. M., editor (1990). Parasites: Immunity and Pathology. The Consequencesof Parasitic Infection in Mammals. London: Taylor & Francis. Bundv, D. A. I’.. Hall. A.. Medlev. G. F. & Savioli. L. (1992). Evaluating measures tocontrolintestinal parasitic infections. World Health Statistics Quarterly, 45, 168-179. Cooper, E. S., Bundy, D. A. I’., MacDonald, T. T. & Golden, M. H. N. (1990). Growth suppression in the Z’richuris dysentery syndrome. European Journal of Clinical Nutrition, 44, 285-291. Elkins, D. B. & Haswell-Elkins, M. (1989). The weight/length profiles of Ascaris Zumbricoides within a human community before mass treatment and following reinfection. Parasitology, 99,293-299. Farthing, M. J. G., Mata, L., Urrutia, J. & Kronmal, R. A. (1986). Natural history of Giardia mfection of infants and children in rural Guatemala and its impact on physical growth. AmericanJournal of Clinical Nutrition, 43,395-405. Freij, L., Meeuwisse, G. W., Berg, N. O., Wall, S. & GebreMedhin, M. (1979). Ascariasis and malnutrition. A study in urban Ethiopian children. American Journal of Clinical Nutrition, 32,1545-1553. Gilman, R. H., Chong, Y. H., Davis, C., Greenburg, B., Virik, H. K. & Dixon, H. B. (1983). The adverse consequences of heavy Trichuris infection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 77,432-438. Greenberg, B. L., Gilman, R. H., Shapiro, H., Gilman, J. B., Mondal, G., Maksud, M., Khatoon, H. & Chowdhury, J. (1981). Single dose piperazine therapy for Ascaris lumbricoides: an unsuccessful method of promoting growth. AmericanJournal of Clinical Nutrition, 34,2508-2516. Gupta, M. C. & Urrutia, J. J. (1982). Effect of periodic antiascaris and antigiardia treatment on nutritional status of preschool children. American Journal of Clinical Nutrition, 36, 79-86. Guyatt, H. L., Bundy, D. A. I’., Medley, G. F. & Grenfell, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology, 101, 139141 _ ._.
Hall, A. (1985). Nutritional aspects of parasitic infection. Propressin Food and Nutrition Science. 9.227-256. Ha& A. & Nahar, Q. (1993). Albendazole as a treatment for infections with Giardia intestinalis in children in Bangladesh. Transactions of the Royal Society of Tropical Medicine and Hygiene, 87,84-86. Hall, A., Anwar, K. S. & Tomkins, A. M. (1992). The intensity of reinfection with Ascaris lumbricoides and its imulications for parasite control. Lancet, 339,1253-1257. Lunn, I’. G. & Northrop-Clewes, C. A. (1993). The impact of gastrointestinal parasites on protein-energy malnutrition in man. Proceedings of the Nutrition Society, 52, 10 l-l 11. Stephenson, L. S. (1987). Impact of Helminth Infections on Human Nutrition. London: Taylor & Francis. Stephenson, L. S., Latham, M. C., Kurz,, K. M., Kinoti, S. N. & Brigham, H. (1989). Treatment with a single dose of albendazole improves growth of Kenyan schoolchildren with hookworm, Trichuris trichiura, and Ascaris lumbricoides infections. AmericanJournal of Tropical Medicine and Hygiene, 41, 78-87. Thein-Hlaing, Thane-Toe, Than-Saw, Myat-Lay-Kyin & Myint-Lwin (1991). A controlled chemotherapeutic intervention trial on the relationship between Ascaris lumbricoides infection and malnutrition in children. Transactions of the Royal Society of Tropical Medicine and Hygiene, 85,523-528. WHO (1990).WHO Model Prescribing Information. Drugs used in Parasitic Diseases. Geneva: World Health Organization.
241
Leading Article Intestinal
parasitic
worms
and the growth
of children
WHO Collaborating Centre for the Epidemiology of Intestinal Parasitic Infections, Department of Biolog_y, Andrew Hall Imperial College, Prince Consort Road, London, S W7 2BB, UK
The popular concept that the food stolen by intestinal worms is responsible for thin children provides an intuitively reasonableexplanation for a direct effect on growth even without considering other, and possibly more important, effects such as impaired digestion and absorption, loss of appetite, gut leakage, and the nutritional costs and physiological consequences of the body’s responses to parasitic infections (HALL, 1985; LUNN & NORTHROP-CLEWES, 1993). But whatever the mechanisms, given that hundreds of millions of children are infected with worms and that many are also wasted and stunted, 2 of the main questions of public health importance are: does periodic treatment of worms reverse any effects on growth and allow catch-up growth to occur? and will enough children benefit to make parasite control a worthwhile intervention to improve child health and growth? In the last few years several studies have shown a beneficial imnact on growth of treating intestinal narasites (GILMAN-et al., i983; STEPHENSENet al., i989; COOPERet al.. 1990: THEIN-HLAING et al.. 1991) but others have not (FR~IJ et al., 1979; GREENBERG et al., 1981; GUPTA & URRUTIA, 1982), and this apparent inconsistency has created some perplexity and ambivalence. There are several biological, nutritional and epidemiological reasons why studies which aim to examine the impact of treating intestinal parasites on the growth of children might not detect an effect. First, many infected children live in environments where they are exposed from birth not only to the infectious stagesof several speciesof intestinal parasites, but to a variety of bacterial and viral diseasesas a result of crowding, contaminated food and water, inadequate sanitation and poor personal hygiene. The nutritional status of such children will reflect not only previous episodes of acute infectious diseasesin addition to concurrent, chronic infections with parasitic worms or protozoa, it will also reflect the adequacy of the diet to support satisfactory rates of growth. The impact of intestinal worms in such circumstances, where each child may have a different historv of infections and diet. will be verv hard to identify in cross-sectional surveys, so prospective studies of growth after treatment are necessary. Second,whether studies are cross-sectionalorprospective. it is inadeauate to classifv children simnlv into 2 groups, infected-and uninfected, as the severity of disease will depend on the intensity of infection. For example, a child with 50 or more Ascaris lumbricoides is much more likely to be diseasedthan one with 5 worms. This important point, which is special to worms, means that infection is not the same as disease. The number of worms necessary for there to be morbidity-a state which is vague and difficult to define for most intestinal worms becauseof a lack of specific signs or symptomswill depend on the speciesof parasite and on factors such as the age,,health and nutritional status of the host. Followmg from this point, even if all children in a community are infected with a speciesof worm, epidemiological studies have consistently shown that the majority are liehtlv infected. This is because intestinal narasites are n&her evenly nor randomly distributed among hosts but tend to be aggregatedin a few heavily infected individuals so that it is not unusual to find 70% of worms in 20% or fewer people (ANDERSON& MAY, 1991). Although such people are in a minority, in communities where the prevalence of infection is high significant numbers are still likely to be heavily infected and may experi-
ence morbidity so that, on a global scale, many tens of millions may be diseased. The aggregation of worms in hosts means that, if an effect on health or growth is to be detected, it will be necessary to stratify subjects by the intensity of infection rather than simply considering them as being infected or uninfected. At the level of the individual, therefore, it is important to assessthe intensity of infection at the time of treatment, either by a faecal egg count or, better still,, by recovering worms after treatment, although this is often impractical. At the community level it is necessaryto appreciate that the relationship between the prevalence of infection and the mean worm burden, an estimate of the intensity of infection in a community, is non-linear. Data from studies around the world on A. lumbricoides, for example, have shown that the mean worm burden is generally low when the prevalence is below about 60%, but may vary greatly when the prevalence is greater than 60% (GUYATT et al., 1990). This means that prevalence is a relatively insensitive indicator of any potential nutritional problem due to intestinal worms and that it is possible to have what may be perceived to be a high prevalence while the averageworm burden is small. A small average worm burden in a community or age class will tend to indicate that few individuals are heavily infected and that few will benefit from treatment. A third important point when considering the impact of intestinal worms is that the duration of infection before treatment is likely to be an important determinant of any growth faltering: a long-standing heavy worm burden is more likely to have had an effect than an equivalent but recently acquired worm load. The life spansof the common intestinal nematodes of humans range from 1 to 4 years (ANDERSON& MAY, 1991) and as individual worms recovered after treatment show a wide rage in size, probably reflecting their ageand the period since infection (ELKINS & HASWELL-ELKINS,1989), hosts probably tend to be infected for long periods with slowly fluctuating numbers of worms. There is no simple technique currently available to quantify such a state without recovering the worms after drug treatment. Fourth, it is necessaryto appreciate what in fact catchup growth presumes: a growth deficit in the first place, an adequate diet after treatment, a sufficient period for catch-up growth to occur, and freedom from disease. The nutritional status of a child before treatment is obviously important because the impact of treating a child of nearlv normal weight and height for age. if all else is equal, i’s likely to bg smaller than if the” child is both stunted and wasted before treatment. It is also reasonable that, if a child is to show catch-up growth after treatment for worms, then the child’s diet must be nutritionallv adequate to support catch-up growth in the first place, and that the child should be free from serious illness which might also impair growth. Such conditions do not always occur after treating children in the settings in which intestinal worms are most common, and heavily infected children are often drawn in the first place from the most deprived and vulnerable sections of the communitv. Because intestinal worms do not seem to orovoke a fully protective immune response in humans (BEHNKE, 1990), reinfection can occur immediately after treatment, although it may take some months before heavy worm burdens are reacquired: a study in Bangladesh of reinfection with A. lumbricoides found that, although treating children every 6 months with an anthel-
242 mintic did not reduce the prevalence of infection, it did serve to reduce mean worm burdens (HALL et al., 1992). In circumstances where the transmission of worms is very intense, it may be necessaryto treat all children repeatedly if catch-up growth is to be detected, and in communities where reinfection is rapid and diets are poor it may take many months and several rounds of treatment for an effect to be observed. A study in Burma of treating children every 3 months for A. Zumbricoides infections found significant increments in height gain after 6 months but significant gains in weight among treated children were observed only after 24 months (THEINHLAING et al., 1991). Fifth, in many communities multiple parasitic infections are the rule rather than the exception, and not all drugs for treating intestinal worms are equally effective: for example pyrantel pamoate, levamisole and piperazine are not effective against Ttichuris trichiuru (WHO, 1990). A selective approach to treatment, although scientifically precise, may be unrealistic, particularly in terms of public health. There are drugs available such asmebendazole and albendazole which are effective treatments for several soecies of intestinal nematodes (WHO, 1990) and single-dosesof albendazole have also been shown to have some effect against Giardia duodenalis (see HALL & NAHAR, 1993), another intestinal parasite associatedwith growth faltering (FARTHINGet al., 1986). Finally, there are someimportant features of study design which need to be recognized. If the impact of treatment is to be dissociated from other influences on growth, then an untreated control group is required (STEPHENSON,1987), and the cases and controls, whether allocated individually or by communities, should be similar in terms of initial parasitic infections and nutritional status. If allocation is done on a community basis, such as by village, then the sample size of villages must also be adequate. Studies which have met these criteria have shown an effect of treatment (STEPHENSONet al., 1989; THEIN-HLAING et al., 1991), but they can pose a dilemma when heavily infected and malnourished children are detected: if such children are excluded from the study on ethical grounds it will introduce a bias against the detection of a beneficial effect. This dilemma, between scientific needs and ethical imperatives, means that ideal studies are difficult to do and will always be easy to criticize if controls are in any way inadequate, so that the null hypothesis that intestinal worms have no effect on the growth of children could be acceptedin studies which fail to show an effect. But most studies which have come to such a conclusion, and it would be invidious or contentious to cite them, can be criticized becausethey are scientifically flawed for one or many of the reasonsgiven above. Unfortunately, because of the enidemioloaical and ethical nroblems of undertaking scientifically falid research this can lead to a position in-which, the cynics may argue, studies showing no effect will be disregarded while onlv those which show an effect will be accepted. Althou h several studies have shown an impact on growth oPtreating intestinal parasitic infections much attention has focused on children less than 5 years old, as this agegroup is considered to be particularly vulnerable. Nevertheless, in many communities the majority of children aged between 5 and 15 years are not only infected with at least one species of worm but they also tend to harbour the heaviest burdens (BUNDY et al., 1992). For these reasons a large proportion of this age group, which has in the past been rather neglected in terms of health care, could benefit during childhood from periodic treatment for worms. There are now available safe, low cost, single dose drugs to treat parasitic worms (WHO, 1990), and the fact that many children
aged 5 to 15 years congregate daily in schools provides a situation and an existing infrastructure in which periodic treatments could be delivered and thereby make a significant contribution to child health. Acknowledgements I thank Don Bundv. Kate Nokes and Fiona Watson for heluful discussions.
’’
References Anderson, R. M. & May, R. M. (1991). Infectious Disease ofHumans, Dynamics and Control. Oxford: Oxford University Press. Behnke, J. M., editor (1990). Parasites: Immunity and Pathology. The Consequencesof Parasitic Infection in Mammals. London: Taylor & Francis. Bundv, D. A. I’.. Hall. A.. Medlev. G. F. & Savioli. L. (1992). Evaluating measures tocontrolintestinal parasitic infections. World Health Statistics Quarterly, 45, 168-179. Cooper, E. S., Bundy, D. A. I’., MacDonald, T. T. & Golden, M. H. N. (1990). Growth suppression in the Z’richuris dysentery syndrome. European Journal of Clinical Nutrition, 44, 285-291. Elkins, D. B. & Haswell-Elkins, M. (1989). The weight/length profiles of Ascaris Zumbricoides within a human community before mass treatment and following reinfection. Parasitology, 99,293-299. Farthing, M. J. G., Mata, L., Urrutia, J. & Kronmal, R. A. (1986). Natural history of Giardia mfection of infants and children in rural Guatemala and its impact on physical growth. AmericanJournal of Clinical Nutrition, 43,395-405. Freij, L., Meeuwisse, G. W., Berg, N. O., Wall, S. & GebreMedhin, M. (1979). Ascariasis and malnutrition. A study in urban Ethiopian children. American Journal of Clinical Nutrition, 32,1545-1553. Gilman, R. H., Chong, Y. H., Davis, C., Greenburg, B., Virik, H. K. & Dixon, H. B. (1983). The adverse consequences of heavy Trichuris infection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 77,432-438. Greenberg, B. L., Gilman, R. H., Shapiro, H., Gilman, J. B., Mondal, G., Maksud, M., Khatoon, H. & Chowdhury, J. (1981). Single dose piperazine therapy for Ascaris lumbricoides: an unsuccessful method of promoting growth. AmericanJournal of Clinical Nutrition, 34,2508-2516. Gupta, M. C. & Urrutia, J. J. (1982). Effect of periodic antiascaris and antigiardia treatment on nutritional status of preschool children. American Journal of Clinical Nutrition, 36, 79-86. Guyatt, H. L., Bundy, D. A. I’., Medley, G. F. & Grenfell, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology, 101, 139141 _ ._.
Hall, A. (1985). Nutritional aspects of parasitic infection. Propressin Food and Nutrition Science. 9.227-256. Ha& A. & Nahar, Q. (1993). Albendazole as a treatment for infections with Giardia intestinalis in children in Bangladesh. Transactions of the Royal Society of Tropical Medicine and Hygiene, 87,84-86. Hall, A., Anwar, K. S. & Tomkins, A. M. (1992). The intensity of reinfection with Ascaris lumbricoides and its imulications for parasite control. Lancet, 339,1253-1257. Lunn, I’. G. & Northrop-Clewes, C. A. (1993). The impact of gastrointestinal parasites on protein-energy malnutrition in man. Proceedings of the Nutrition Society, 52, 10 l-l 11. Stephenson, L. S. (1987). Impact of Helminth Infections on Human Nutrition. London: Taylor & Francis. Stephenson, L. S., Latham, M. C., Kurz,, K. M., Kinoti, S. N. & Brigham, H. (1989). Treatment with a single dose of albendazole improves growth of Kenyan schoolchildren with hookworm, Trichuris trichiura, and Ascaris lumbricoides infections. AmericanJournal of Tropical Medicine and Hygiene, 41, 78-87. Thein-Hlaing, Thane-Toe, Than-Saw, Myat-Lay-Kyin & Myint-Lwin (1991). A controlled chemotherapeutic intervention trial on the relationship between Ascaris lumbricoides infection and malnutrition in children. Transactions of the Royal Society of Tropical Medicine and Hygiene, 85,523-528. WHO (1990).WHO Model Prescribing Information. Drugs used in Parasitic Diseases. Geneva: World Health Organization.