Original Articles

Indian Pediatrics 2000;37: 19-29

Effectiveness and cost-effectiveness of albendazole in improving nutritional status of pre-school children in urban slums

Shally Awasthi, Vinod Kumar Pande and Robert H. Fletcher

From the Department of Pediatrics and Institute of Clinical Epidemiology, King George's Medical College, Lucknow (U.P.), India and Department of Ambulatory Care and Prevention, 126 Brookline Avenue Suit 200, Boston MA, 02215, U.S.A.
Reprint requests: Dr. Shally Awasthi, C-4, Officer's Colony, Niralanagar, Lucknow (U.P.), 226 020, India. e-mail: <[email protected]>
Manuscript received: April 28, 1999; Initial review completed: May 18, 1999; Revision accepted: July 26, 1999.

Objective: To study the clinical efficacy and the incremental cost-effectiveness of albendazole in improving the nutritional status of pre-school children. Design: Single blind, placebo-controlled trial with child as the unit of randomization. Setting: In the Anganwadi centers of the Integrated Child Development Services situated in the urban slums of Lucknow, North India. Methods: Thirty-two Anganwadi centers were randomly selected for the trial. Included were registered resident children between 1.5 to 3.5 years of age with informed and written parental consent. The intervention group received 600 mg of albendazole powder every six months while the placebo group received same quantity of calcium powder. Enrolled children were contacted once in six months from January 1995 to 1997 and given treatment. The outcome measure were change in the proportion of underweight (weight for age <-2.00z), stunted (height for age <-2.00z) children and the cost per child prevented from becoming stunted. Results: There were 610 and 451 children in the albendazole and placebo groups, respectively. Mean age at recruitment was 31.8 months (SD: 9.7). Follow-up and compliance in both the groups was >95%. During the 2 year follow-up, the proportion of stunted children increased by 11.44% and 2.06% in the placebo and albendazole groups, respectively, and the difference was 9.38% (95% CI 6.01% to 12.75%; p value <0.0001). Direct fecal smear was positive for the ova of ascaris in 41.2% and 55.3% children in the albendazole and placebo groups, respectively at the end of the study (p value <0.001). The annual family expenditure on illness in the recruited child was Rs. 743 (SD: 662) and Rs. 625 (SD: 609) in the albendazole and the placebo groups, respectively. The incremental cost-effectiveness ratio was Rs 543.00 for each case of stunting prevented with albendazole. There was no difference in the various morbidity or cognitive performance, as judged by the revised Denver prescreening questionnaire, in both the groups at enrollment as well as at the end of the study. Conclusions: Six monthly albendazole reduces the risk of stunting with a small increase in the expenditure on health care from the payer's perspective. Larger trials are needed to study the effect of albendazole on prevention of stunting, cognitive functions and all-cause childhood mortality.

Key words: Albendazole, Cost-effectiveness, Efficacy, Nutritional indices, Trial.

The majority of pre-school children in India are malnourished(1) and also worm infested(2). The most common geohelminth infesting pre-school children in the urban slums of Lucknow is ascaris(3) and similar findings have been reported from various developing countries(1,4-5). Infestation with ascaris has been associated with malnutrition(4,6-9) and may be its cause. We hypothesized that periodic deworming of children will result in an improvement of their nutritional status and that this will result in a reduction of expenditure on their health care. We used albendazole for deworming because it has been found to be effective against almost all the geohelminths(10-13), with cure rates of >90% for Ascaris lumbricoides.

Methods

Setting and Subjects

The study was carried out in the urban slums of Lucknow, North India, from January 1995 to 1997. This setting has been described in details elsewhere(14). Through the national Integrated Child Development Scheme (ICDS) each slum has an "Anganwadi Center" (AC) with one health worker ("Anganwadi" Worker) and caters to the needs of children under 6 years of age. The "Anganwadi" worker maintains an almost complete list of the beneficiaries.

Eligible children were those between 1.5 to 3.5 years of age who were registered with the "Anganwadi" worker and whose parents consented to the study. No parent refused to participate. It was assumed that majority of children below 1.5 years of age would not be harboring intestinal parasites, and therefore would not be benefited by deworming. Hence children only above 1.5 years were eligible for the study. To minimize loss to follow-up children above 3.5 years were not included as they would no longer be registered with the Anganwadi worker at the end of this 2-year study. The institutional ethics committee cleared the study.

There were approximately 200 functional urban slums in Lucknow in 1995. Of these, 50 have been participating in an ongoing trial since 1994(15). From the remaining 150 urban slums, 32 were randomly selected for this study. A list of all the eligible children from a slum was obtained. Maintaining the order in which the Anganwadi worker within a slum listed it, each child was allocated a serial number. Those with odd or non-zero endings numbers, approxi-mately 40% of all eligible candidates, were assigned to the placebo and the rest to the intervention group. Thus, from 32 slums 1061 children were enrolled in the study. Personal interviews of mothers were done to collect information on the socio-economic status of the family and history of passage of worms in the preceding 1 month in the enrolled child.

Intervention

As a part of the usual health maintenance, children are supposed to be weighed once every six months. Our intervention was linked with these visits. Children randomized to the inter-vention group were given 600mg of albendazole powder every six months for 2 years, while those in the placebo group received the same quantity of calcium powder. The two powders looked and smelled almost the same but were different in taste. The mothers dissolved the powder in water and the children were made to swallow it in front of the project officer. Those children who could not take the medicine in front of the project team were allowed to take it home. The next day the same project officer contacted these mothers to assess compliance. The mothers were blinded to the intervention type but not the providers.

Outcome Measures

The primary outcomes were changes in the prevalence of underweight and stunted children over two years. "Underweight" was defined in relation to the World Health Organization's standards (National Center for Health Statistics) for nutritional anthropometry as those with a weight for age `z' score <_2.00. Stunted were children with height for age `z' score <-2.00. Change in the prevalence of wasting was also assessed, where wasting was defined as weight-for-height <_2.00 `z' score.

Secondary outcomes were weight and height gains, hemoglobin levels, illness epi-sodes, developmental status and passage of worms. The number of deaths in each group also has been reported, although death was not a main outcome for this study.

Assessment of Age

Mothers gave information on the age of the child. The field officers validated the age with an event calendar of the relevant year. Age was corrected to the nearest month. One-third of the anganwadi workers also had data on either the birth date or the age of the child. Child's age as told by the mother was validated against the age information available with the Anganwadi wherever possible. If there was a discrepancy of more than 1 month between the two sources of information then, for uniformity, the information given by the mother was taken as correct for the purpose of analysis. For computer analysis, data was entered by the exact month. If the day within the month was not known, then the day was entered as 15th of the corresponding month.

Nutritional Assessment

Four-trained graduate field workers did this. Children were weighed on a electronic digital weighing scale that could measure up to the nearest 100 grams. Inter and intra-observer variation was less than 5%. The calibration of the machine was validated against standard weights of 10 kg and 20 kg weekly. The cor-relation coefficient was 0.96 with the standard weights. Recumbent length was measured in children less than 2 years of age on an infantometer. For children older than 2 years of age height was measured using the Leicester height measure stadiometer. The infantometer and stadiometer could measure to a minimum of 1 mm. Inter and intra-observer variation was less than 5%. An independent project officer then validated approximately 10% of weight and height measures within 1 week of the initial survey. The correlation between the initial weight measure and the validated measure was 0.91. If the two readings of the same child differed by more than 200g, a mean of the two was used in the analysis. A single project officer estimated the hemoglobin levels by visual color estimation using Sahli's hemoglobinometer(16) in the slum. While we calibrated the instrument weekly, validation of hemoglobin level was not done.

Parasitology

Mothers were asked to recall passage of roundworms by the child in the six months before entering the study. They were instructed to collect fresh fecal specimen of the child in a labeled glass vial provided. The intervention was given only after the stool specimen had been collected. Within 8 hours of collection direct smear examination was done for ova of helminths and saline iodine staining for the detection of protozoa(17). The intensity of infestation was not estimated. The technician was blind to the randomization status.

Development Assessment

We used the revised prescreening Denver Questionnaire (RPDQ)(18) for assessing the developmental status of the children. R-PDQ is in English and was translated to Hindi and pilot tested for understandability. Literate mothers were encouraged to self-administer the R-PDQ.

Illiterate mothers were administered R-PDQ by the project officers in accordance with the manual(18,19).

R-PDQ was assessed at baseline and at the end of 2 years' follow-up. The physician was blind to the type of intervention given to the child. Those who could not perform more than 2 tasks, which could be done by 90% of children the same age, have been classified as having a "questionable" developmental status.

Assessment of Illness Episodes

The mothers were asked to recall the illnesses their child had suffered from in the preceding month. The illnesses were catego-rized into respiratory, diarrheal, dysentery, skin infections and fever. The definitions of various illnesses have been given elsewhere(14,20).

Cost Outcomes

The cost outcome was direct medical cost of illness from the family's (payers') pers-pective. Incremental cost effectiveness ratio was calculated for cases of stunting prevented by albendazole.

Cost data collection: Information was collected on whether medical resources had been used for the child in the preceding month. The resources considered were the health care provider's service, medicines, laboratory investigations and hospitalizations. The cost of a resource was what they actually paid for it. Lastly, the morbidity leading to medical resources consumption was assessed.

Analysis

The sample size calculations were based on a 60% prevalence of underweight or stunting at baseline. Assuming that there would be no change in the proportion of underweight or stunted children with the placebo and a 15% improvement with albendazole, then to detect this difference with an alpha of 5%, power of

80% and 1:1 randomization we would need 500 children in each arm of the trial.

We assessed loss to follow-up, compliance and crossover in the two arms of the trial at each of the three follow-up visits by univariate analysis using Chi-square test. Baseline demo-graphic, religion, socio-economic, immuniza-tion, nutritional and developmental status of children randomized to the two groups of the trial were compared using chi square test for categorical and Student `t' test for continuous variables.

Epi Info6 statistical software(21) was used for nutritional anthropometry calculations. Anemia was defined as hemoglobin less than 11g/dl(22). The proportion of underweight, stunted, wasted and anemic children as well as those with questionable development status in the two groups of the trial at baseline were compared in the two arms of the trial using the Chi-square test.

Univariate comparison of weight and height gains over 2 years in the two groups was done by student's test. The differences in the weight and height gains between the albendazole and the placebo group were considered in the primary analysis since each child served as a control for him/her self in both the arms. The analysis did not take into account non-independence of children, slums and family members.

Within each arm, changes in the proportion of underweight, stunted and wasted children at the end of the trial were compared using Chi square test. The difference in the change of proportion of the nutritional indices between the placebo and the albendazole arms along with the 95% confidence interval of the difference was calculated.

Univariate comparison of hemoglobin levels, developmental delay and the incidence density (ID) of various illnesses per 100 child-years in the intervention and control groups was done using Student's test for continuous and Chi-square test for categorical outcomes. For measles, we have reported the incidence rate only.

Cost Analysis

Inter-and intra-group comparisons were done on the estimates of monthly family spending on illnesses by using the analysis of variance. Since there was no intra-group variance in the monthly cost estimates, the annual cost was taken as twelve times the average monthly cost of illness within each group. The annual cost was compared in the two arms of the trial using Kruskall-Wallis test. Using a 2-tailed distribution, a p value of <0.05 was considered statistically significant.

Cost Effectiveness Analysis

Incremental cost-effectiveness, where effectiveness is prevention of stunting was done for a hypothetical cohort of 10,000 children, randomized to the albendazole and placebo groups in a 1:1 ratio. The values used for the risk reduction of stunting with albendazole at the end of 2 years were the same as observed in the trial.

The incremental cost effectiveness ratio was calculated using the following formula:

Discounted TC* (albendazole-placebo) + intervention cost /{st2(placebo - albendazole)}

where, TC = Total annual cost, albendazole = albendazole group, placebo = Placebo group, and st2 = # stunted children at the end of 2 years. In this calculation we used 2-year annual cost. The second year costs were discounted by 10% since there is a high rate of inflation in India. For sensitivity analysis of clinical effects of stunting, we have used the mean and 95% upper and lower estimates of albendazole and placebo effects. Considering the 2-year discounted costs  of this trial, we report the incremental cost effectiveness ratio for each case of stunting prevented for both the combinations.

Results

We recruited all the eligible children between the ages of 1.5 to 3.5 years (n=1061) registered with the anganwadi worker from 32 randomly selected Anganwadi centers. Of these 52% were males and 48% were females.

We enrolled 610 and 451 children in the albendazole and placebo groups, respectively. At the end of the study, 9 children in the albendazole and 7 in placebo group had been lost to follow-up. Seventy-six and seventy two per cent children in the albendazole and placebo groups, respectively, took the intervention in front of the project officer. Most of the mothers of children who were sent home with the medicine said that the child took it. On combining the number of children who took the intervention in the community and those who took it at home, we found 95.9% and 96.9% compliance in the albendazole and placebo groups, respectively.

The project workers noted at each visit the intervention type given to each subject. At the first, second and third follow-up visits, 7.5%, 12.6% and 14.5% children, respectively, from the placebo group were offered albendazole.

Baseline Characteristics

The mean age was 31.8 mo (SD 9.7 mo); sixty seven per cent subjects were Hindus and thirty three per cent Muslims. The character-istics of children in the two group of the trial are shown in Table I. A similar proportion of children in the intervention and control groups were undernourished and had a history of worms at the time they entered the study. Of the 1061 children, 285 (26.9%) were siblings of which 97 (34%) and 71 (24.9%) were random-ized to albendazole and placebo groups, respectively, and 117 (41.1%) were in either of the two groups.

Table I^__Characteristics of the Participants at Enrollment and at the End of the Study

Figures in parantheses indicate percentages. Values depict either mean � SD or number.

* P = 0.03; ⁺ P = 0.05 ⁺⁺ <0.0001.

Clinical Efficacy

The weight and height and changes in these two parameters over the study period are shown in Table I. The main outcome measures, the risk reduction of being underweight or stunted, are summarized in Table II. Of 53.8% children with a normal and 46.2% questionable R-PDQ assessment at baseline, there was almost no change in the proportion who were assessed to be developmentally normal in the albendazole and placebo groups, respectively, at the end (Table III).

Table II^__Assessment of Change in Nutritional Indices over 2 Years

Abbreviations:
For intra-group comparison of pre and post trial values
^a = p value < 0.001; ^b = p value < 0.001; ^c = p value < 0.001; ^d = p value = 0.5

Table III^__ Risk Reduction of Having a Questionable R-PDQ Assessment.

Morbidity

There was no difference in the morbidity due to respiratory and diarrheal diseases and those due to skin infections, high fever and miscellaneous causes (Table IV). The incidence rate of measles was 2.4 (95% CI 1.4 - 3.9) versus 0.4 (95% CI 0.07 - 1.5; p value = 0.01) in the albendazole versus placebo groups. There were 11 deaths in 2 years, 7 in albendazole and 4 in the placebo arm.

Table IV^__ Incidence Density per 100 Child Years for Various Infections (Mean, SD)

   None of the differences between the groups were significant (p > 0.05).

Cost Outcomes

The medical resource consumption by the sick subjects has been described elsewhere(20). The annual expenditure was Rs 743 (SD 662) and Rs 625 (SD 609) (Kruskal-Wallis test p value = 0.1) in the albendazole and placebo groups, respectively. The cost of various illnesses has been given elsewhere(20).

For calculating the incremental cost-effectiveness ratio for two years of six monthly treatment with albendazole the market price of the intervention of Indian Rupees (Rs. 20/- per dose) has been used. The incremental cost of treating 5000 children with albendazole with the data from this trial is Rs. 122091, which includes the market price of the intervention. With the mean albendazole and placebo effects, the incremental cost-effectiveness ratio was Rs. 543 for each case of stunting prevented with albendazole, respectively.

The cost effectiveness ratio was sensitive to the clinical effects of albendazole and placebo. With the 95% upper albendazole and placebo effect and 95% lower albendazole and placebo effect, the incremental cost-effective-ness ratio per case of stunting prevented was Rs. 498 and Rs. 629.

Discussion

The present study was a community based, randomized placebo controlled, single blind trial for assessing the clinical efficacy and costs of albendazole in preventing underweight and stunting in pre-school slum dwelling children. There was a statistically significant reduction in the proportion of children who become stunted at the end of 2 years with six monthly albendazole. The incremental cost effectiveness ratio with mean albendazole and placebo effect was Rs. 543 for each case stunting prevented by albendazole using just the direct medical costs and the cost of intervention. The cost-effectiveness ratio was sensitive to clinical efficacy of albendazole and placebo.

There were certain advantages and dis-advantages of our community based study design. We found almost negligible migration out of the urban slums for the groups as a whole, so there was almost complete follow-up. However, being a single blind trial, the project workers did succumb to community pressure and occasionally changed the intervention type given. Sometimes children passed round- worms within a couple of days after ingestion alben-dazole and this unblinded the parents. Therefore, as expected the crossover were less from the albendazole to the placebo group than vice-versa. Crossover to the placebo group may be intentional on the part of the project officers to compensate for albendazole substitution in others as the total doses of interventions given to them were fixed. Since the trial was analyzed as intention to treat, these crossover biased the result towards finding no effect. However, since the study was single blind, there is a possibility of bias towards the positive side, despite taking all precautions to keep the primary hypothesis unknown to the field staff. Children between 1.5 to 3.5 years were included in the trial and hence the results of the work have to be validated for other age groups and different sites before generalization.

We found an imbalance in the measles immunization status, with a better coverage in the placebo than the albendazole group. This did result in a greater number of cases of measles in the albendazole group. Childhood morbidity are known to increase after measles(23) and measles also aggravates malnutrition(23). This imbalance at baseline can partly explain the

increased annual expenditure on illness in the albendazole groups. Since we did not look for the causes of reduced measles vaccination coverage in the albendazole arm in this study, it is not possible for us to state whether this imbalance was just by chance.

The sample size for this study was based on categorical outcome. Over 2-year follow-up a statistically significant increase of 11.44% and 2.06% of stunting was noticed with placebo and albendazole, respectively. Demonstrating differ-ences in the change of nutritional indices is more important than merely weight or height gains as the former can be directly translated into community benefits while the value of the latter two parameters in isolation is unclear. To detect a 0.5 cm difference in height gain with a standard deviation of 0.5 cm, a three times larger sample size would be required in each arm as compared to the current one(24). Hence, the current study can neither prove nor disprove any effect of the intervention on height gain, a continuous outcome. Various workers from different countries have demonstrated a weight gain with albendazole(8,9) and other anthel-minths(2). In another randomized trial of six monthly albendazole in pre-school children in the urban slums of Lucknow a 35% greater weight gain was noticed with albendazole(15). However, unlike the current study, randomized by area was done in the previous study. Randomization by area avoided crossover.

Demonstrations of height gain with periodic deworming of children have been inconsis-tent(8,9,15). From a policy perspective, changes in the community prevalence of stunting have hardly ever been measured as in the current study. The present study failed to demonstrate any improvement in the hemoglobin levels with periodic albendazole therapy and to demonstrate any beneficial effect of routine de-worming on cognitive performance of children. Cognitive assessment in this study was a secondary objective and sample size was not adequate to pick up small changes in it with routine de-worming. Various other workers, however, have shown inconsistent effects on cognitive per-formance of routine de-worming(25,26).

The average income of majority of the families was Rs. 1000 per month. Thus, each family spent 5% to 10% of its income on health of preschool children(20). Using the mean albendazole and placebo effects, each case of stunting prevented will cost Rs. 543 or <5% of annual family income. We have also found that with routine deworming the prevalence of fecal smear positivity for ascaris increased to 41.2% from a baseline level of 12.5%. This indicates high re-infection rates. In children with placebo, there was an increase of the prevalence of fecal smear positivity for ascaris from a baseline level of 10.6% to 55.3%. These prevalence rates in placebo group are in accordance to those found in the routinely dewormd group and may be indicative of high transmission rate. Since parents were neither encouraged or discouraged from de-worming their children, there is a possibility of underestimation of parasite prevalence in both the groups, but more so in the placebo. The data from the trial justifies mass deworming of pre-school children since about half of them are infested with round worms. If the deworming medicine were supplied at cost price or at subsidized rate, it would be seem to be an attractive option for prevention of stunting from the payer's perspective. Currently in the urban slums of Lucknow supplemental diet is being used for improving the nutritional status of preschool children and is being distributed through the ICDS system. Routine deworming can also be considered as an additional strategy.

A recent meta-analysis on the effects of deworming on nutritional and cognitive para-meters was done by the Cochrane Collabora-tion(27). Meta-analysis showed small statistically significant effects on mean change in weight in single and multiple dose trials less than one year in duration but not in programs longer than one year. Narrative analysis indicates mixed and inconclusive results related to effect on cognitive performance. Although there is a general belief that treating intestinal parasite infections in children will improve growth and cognitive performance, there is no current evidence to quantify these effects(27).

We conclude that in the urban slum children routine deworming reduces the risk of stunting in preschool children with considerably low incremental cost. Similar studies have to be replicated in other parts of India and other developing countries for generalizability.

Acknowledgement

We would like to thank Prof. Sankey Wiliams and Mr. Henry Glick, Department of General Internal Medicine, Hospital University of Pennsylvania, Philadelphia, USA, for their assistance in protocol development. The finan-cial support for this study was provided by the International Clinical Epidemiology Network (INCLEN), Philadelphia, USA through its grant # 2002-94-62-3 under the Clinical Economics Small Grants Program.

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