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© 2007 American Society for Nutrition J. Nutr. 137:1455-1459, June 2007

Community and International Nutrition

Benefit of Vitamin A Supplementation on Ascaris Reinfection Is Less Evident in Stunted Children1,2

Leslie G. Payne3,4, Kristine G. Koski3,*, Eduardo Ortega-Barria5 and Marilyn E. Scott3,4

3 School of Dietetics and Human Nutrition and 4 Institute of Parasitology, McGill University (Macdonald Campus), Quebec H9X 3V9, Canada and 5 Instituto de Investigacion Cientifica Avanzadas y Servicios de Alta Technologia (INDICASAT), Panama City, Panama

* To whom correspondence should be addressed. E-mail: kris.koski{at}mcgill.ca.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Despite the common coexistence of vitamin A deficiency and Ascaris infection in preschool children in developing countries, and despite the widespread use of vitamin A supplements, remarkably little is understood about the impact of vitamin A supplementation on this gastrointestinal nematode. The Ministry of Health of Panama recently initiated a vitamin A supplementation program in rural indigenous populations. We took advantage of this initiative to assess the benefit of 200,000 IU (60 mg retinol) vitamin A on reinfection with Ascaris following deworming. Baseline stool exams, anthropometry, and socio-economic data were collected for 328 preschool children from 12–60 mo of age (106 supplemented within previous 3 mo and 222 unsupplemented within previous 6 mo). All children were dewormed with albendazole, and reinfection levels were monitored 3 and 5 mo later. Baseline prevalence of Ascaris was 79.5%. Stepwise regression showed that Ascaris intensity was lower in Vit A-supplemented children at baseline and 3 mo after deworming, but not after 5 mo. As 61% of the children were stunted, the impact of supplementation on Ascaris reinfection was examined separately for stunted and children of normal height. Prevalence and intensity of Ascaris at baseline and 3 mo after deworming were lower in children of normal height, but in stunted children the benefit was restricted to those who were dewormed within 6 wk of supplementation. Our study provides evidence that combined vitamin A supplementation and deworming reduces Ascaris reinfection in children living in areas of chronic parasitosis, but that the duration of the benefit is less in stunted children.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Malnutrition and intestinal parasitism, leading causes of worldwide morbidity and mortality, have long coexisted in populations where poverty perpetuates conditions of poor housing, low levels of education, poor health services, inadequate sanitation, and poor access to adequate food (1,2). Independent health implications of vitamin A deficiency and of Ascaris lumbricoides (Nematoda) are well documented, but our understanding of their biological interactions is limited, despite their common co-occurrence in the same child. Adult Ascaris worms impair the absorption of vitamin A and fat (3,4), leading to nutritional deficiencies, whereas vitamin A deficiency may reduce the immune response to intestinal parasites (5), leading to higher worm burdens.

Anthelmintic drug treatment is a commonly used intervention to control Ascaris infection, and megadose vitamin A supplements are recommended to reduce vitamin A deficiency (6,7). In areas where Ascaris is endemic, repeated anthelmintic treatment is suggested, as rapid reinfection results in infections that reach pretreatment levels within as little as 4–6 mo (8,9). Unfortunately, such frequent anthelmintic treatment may promote the selection of drug-resistant parasites (10). Megadose vitamin A supplements [200,000 IU retinyl palmitate (60 mg retinol)] can improve vitamin A status for 4–6 mo (6); thus it is recommended that supplements be administered at least every 6 mo to achieve a sustainable impact on the serum retinol concentrations in deficient children (6).

WHO (2004) recently recognized that providing vitamin A supplements and deworming together improves the cost-effectiveness of health delivery as well as compliance (7), but their potential synergistic effects on health have not been well documented. Studies investigating whether deworming enhances the benefit of increased intake of vitamin A, ß-carotene–rich foods (11,12), or vitamin A supplements (13,14) on serum retinol concentrations have provided inconsistent results. This variability has been attributed to the selection of study populations at low risk of vitamin A deficiency or with a low prevalence and/or intensity of Ascaris. Surprisingly, none of these studies investigated the effectiveness of combined interventions on Ascaris reinfection rates.

The purpose of the present study was to investigate whether Ascaris reinfection rates at 3 and 5 mo post anthelmintic treatment would be lower in preschool children who received vitamin A supplementation than in those who had not. The study was conducted in a population of indigenous preschool children in Panama where intestinal nematodes are common, where vitamin A deficiency is a recognized problem, and where acute malnutrition is infrequent but where chronic malnutrition begins at an early age leading to stunting (15). The children in this study were of the Ngöbé indigenous group, living on the outskirts of the formally recognized indigenous regions called comarcas in the Bocas del Toro province of Panama. Although 1–5 y–old children in the comarcas have been eligible to receive 200,000 IU of retinyl palmitate (60 mg retinol) every 6 mo through the Ministry of Health (MOH),5 it was only recently that the MOH began to provide vitamin A supplements to indigenous children outside the comarcas region. We were fortunate to conduct our research just as the distribution of supplements by MOH outreach health teams outside the comarcas was beginning, and where coverage was far from complete. This enabled us to compare unsupplemented with supplemented children without the ethical dilemma of withholding supplements from children who would otherwise receive them.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
This prospective community-based study was designed to monitor Ascaris reinfection of supplemented and unsupplemented children at 3 and 5 mo after deworming of all children. Ethics approval was obtained from the Institutional Review Board of McGill University, the Panamanian Ministry of Health, and the community leaders in the Bocas del Toro province of Panama.

We recruited 595 Ngöbé children aged from 12–60 mo. Each parent or guardian gave written and verbal consent in the presence of a witness. At baseline, a standardized questionnaire administered through an interview with the child's primary caregiver assessed demographic characteristics of the household, household living conditions, and the health status of the child (number of episodes of diarrheal disease and respiratory infections in previous mo, and any chronic diseases or medications). Each child's vaccination card was examined to determine whether the child had received a vitamin A supplement as recorded by the MOH, and if so, the date of supplementation. Anthropometric measurements were taken using standard techniques (17) and age was recorded according to the birth date on the child's immunization card. Height-for-age, weight-for-age, and weight-for-height Z-scores were calculated using EPIinfo, 2002 (CDC), and children were classified as stunted if their height-for-age was ≤2 SD, as underweight if their weight-for-age was ≤2 SD, or as wasted if their weight-for-height was ≤2 SD.

Each caregiver was given a labeled plastic container and verbal instructions on how to obtain fecal samples. The sample was collected the following morning by a community health promoter and transported to the laboratory, where it was examined in duplicate using the Kato-Katz technique (16). The number of parasite eggs per gram (epg) of feces was recorded for each nematode species. Diarrhetic samples were not analyzed; instead a second sample was collected once the diarrhea had subsided. To determine the degree of vitamin A deficiency in the children and to confirm that vitamin A supplementation had improved serum retinol levels, blood samples were collected from a random subsample of supplemented (n = 36) and unsupplemented (n = 29) children at baseline. Using a heel or finger prick technique, a drop of blood was deposited onto filter paper, dried, stored in a Ziploc bag with a dessicant at 4°C until transported to the laboratory where it was stored at –20°C with dessicant. Duplicate dried blood spots were analyzed for serum retinol using HPLC at Craft Laboratories using a standardized technique (18).

We then dewormed all children with 400 mg albendazole, which has high efficacy against Ascaris infection and has the advantage of being effective as a single oral dose (10,19). At 3 and 5 mo after deworming, stool samples were collected from all children, and nematode epg were measured. At the end of the study, all children were given a second dose of 400 mg albendazole and those children who had not received a vitamin A supplement within 6 mo of the final visit received 200,000 IU of retinyl palmitate upon presentation of their vaccination card.

Children were excluded from the study if they showed visible signs of vitamin A deficiency based on an ocular exam conducted by medical students doing their community rotation (n = 0). They were excluded from the data analysis if they received vitamin A supplementation between 3 and 6 mo prior to deworming (n = 43), if they had received anthelmintic treatment within the 4 mo prior to drug treatment (n = 29), if they received either vitamin A supplementation (n = 13) or anthelmintic treatment (n = 71) during the 5 mo follow-up period, or if a full set of data were not available (n = 111). A total of 328 preschool children were included in the data analysis. They were classified as vitamin A supplemented (Vit A+, n = 106) if they received vitamin A within 3 mo prior to the baseline measurements, or as unsupplemented (Vit A–, n = 222) if they had not received vitamin A within the previous 6 mo.

All statistical analyses were carried out using SAS, version 8 (SAS Institute). Baseline demographic and health factors were compared between supplemented and unsupplemented children using a t test or {chi}2 analysis. Ascaris epg were normalized by ln transformation, ln (epg + 1). Repeated measures ANOVA was used to determine whether the pattern of ln-transformed epg over time differed between Vit A+ and Vit A– supplemented children. Stepwise regression analyses were undertaken separately at baseline and at 3 and 5 mo after deworming, using Ascaris ln-epg as the dependent variable. Any independent variable with P > 0.10 was considered nonsignificant and excluded from the model. The impact of stunting was examined using linear regression analysis of both the height-for-age Z-score and the interval between vitamin A supplementation and deworming using Ascaris ln-epg as the dependent variable. Prevalence was compared between stunted and normal height children using 95% binomial confidence limits, and ln-epg was compared using 1-way ANOVA controlling for age and income. Values are means ± SE, and differences were considered significant at P < 0.05.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
Our baseline interviews showed that Vit A+ and Vit A– children lived in households of similar size with mothers who had comparable years of schooling; however, household income and access to latrines were higher in Vit A+ than in Vit A– children (Table 1). Caregivers of both groups reported similar frequency of diarrhea and respiratory tract infections. Chronic malnutrition was equally common in Vit A+ and Vit A– groups, with 61% of children stunted and 28% severely stunted (≤–3 SD from mean height-for-age Z-score); in contrast, only 15% were underweight and <1% were wasted (Table 1). Serum retinol concentration in Vit A– children, 0.56 ± 0.03 µmol/L (n = 29), was below the WHO cutoff for vitamin A deficiency (0.7 µmol/L) (17), whereas that in children who had received vitamin A within the past 3 mo was 0.81 ± 0.09 µmol/l (n = 36). The most common parasite, Ascaris lumbricoides, was present in the fecal samples of 79.5% of children at baseline with an intensity of 21494 ± 2500 epg. Due to the low prevalence and intensity of Trichuris (19% infected, 103 ± 45 epg) and hookworms (<1% infected), subsequent analyses focused on Ascaris. Repeated measures ANOVA revealed significant effects of time (F2, 652 = 88.43, P < 0.0001) and vitamin A supplementation (F1, 326 = 20.29, P < 0.0001) on Ascaris ln-epg. Stepwise regression analyses were then conducted using data from baseline and 3 and 5 mo after deworming, with Ascaris ln-epg as the dependent variable, and supplementation, as well as other potential predictors of Ascaris infection and reinfection, as independent variables (Table 2). The absence of vitamin A supplementation entered as a highly significant predictor of Ascaris ln-epg both at baseline and at 3 mo after deworming, but not after 5 mo. Among demographic factors, the age of the child was significant at baseline, whereas the number of people in the household was significant at 3 mo, and mother's education was a predictor of Ascaris ln-epg at 5 mo. Surprisingly, neither household income nor access to latrines predicted Ascaris ln-epg. Among health factors, a low frequency of diarrheal episodes entered as a predictor of Ascaris ln-epg at baseline, and children with higher Ascaris ln-epg at baseline had a higher ln-epg 5 mo after deworming. Finally, low height-for-age was a highly significant predictor of Ascaris reinfection both at 3 and 5 mo after deworming. Linear regression confirmed that Ascaris ln-epg at 3 mo after deworming increased with decreasing Z-scores, indicating that reinfection occurred more rapidly in more severely stunted children (P = 0.0071).


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  		TABLE 1 Baseline characteristics and living conditions of Vit A+ and Vit A– Panamanian preschool children for whom a complete data set is available1

 

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  		TABLE 2 Predictors of Ascaris ln epg in Panamanian preschool children at baseline and at 3 and 5 mo following deworming based on stepwise regressions

 
Given the importance of stunting that emerged in the regression analyses, we considered in more detail the impact that stunting might have on infection and reinfection. At baseline, stunted children had a higher intensity of Ascaris infection compared with normal height children (P = 0.008), which persisted at both 3 mo (P = 0.0191) and 5 mo (P = 0.0019) postanthelmintic treatment. Interestingly, the impact of vitamin A supplementation on Ascaris prevalence and intensity differed markedly between stunted and nonstunted preschool children (Fig. 1). Among nonstunted children, baseline prevalence and intensity of infection was significantly lower in Vit A+ children than in Vit A– children. Similarly, at 3 mo after deworming, reinfection rates in children of normal stature were reduced in vitamin A–supplemented children. In contrast, among the stunted children, vitamin A supplementation had no detectable benefit on prevalence or intensity at baseline or on rates of reinfection at 3 mo. As expected, after 5 mo, vitamin A supplementation lost its effect on Ascaris prevalence and intensity regardless of the child's height-for-age.


Figure 1
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  		FIGURE 1  Ascaris prevalence (A) and intensity (B) at baseline and at 3 and 5 mo after anthelmintic treatment (indicated by vertical dashed line) in growth-stunted and normal height Panamanian preschool children. Values are percentage ± 95% CI (A) and mean ± SEM (B), n = 62 stunted, supplemented children; n = 44 normal height, supplemented children; n = 147 stunted, unsupplemented children; n = 75 normal height, unsupplemented children. Analysis of the data in Figure 1B involved a set of 1-way ANOVA controlling for age and income at each time point and within each height stratification. Different lowercase letters indicate significant differences between supplemented and unsupplemented children within height stratifications at each time point, P < 0.05.

 
To confirm the modifying effect of stunting on the ability of vitamin A supplementation to delay reinfection, we evaluated whether the interval between vitamin A supplementation and anthelmintic treatment influenced reinfection rates among the subset of children who received a supplement. None of the children of normal stature who were dewormed within 6 wk of receiving vitamin A were reinfected at 3 mo, and linear regression analysis further substantiated this observation by showing that 3-mo reinfection rates increased as the interval between supplementation and deworming increased (P = 0.0046) even in preschool children of normal height. Moreover, stunted children who received vitamin A within 6 wk of deworming had a lower 3-mo reinfection epg (ln-epg, 1.8 ± 0.6) than stunted children who received the supplement between 6 and 12 wk prior to deworming (ln-epg, 4.8 ± 0.6) (P = 0.0141).


   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Given the reported negative effects of vitamin A deficiency on immune responsiveness (20,21), we hypothesized that Ascaris intensity at baseline and at 3 mo post-deworming would be reduced in Vit A+ children. We also hypothesized that the beneficial effect might be lost by 5 mo post-deworming, given that it is recommended that megadose vitamin A supplements be given every 4–6 mo (6). The first major finding from our study was that vitamin A supplementation was a significant predictor of lower Ascaris epg not only prior to deworming, but also 3 mo after deworming. Our findings at baseline are consistent with reports of a negative correlation between serum retinol and Ascaris epg in regions where vitamin A deficiency and Ascaris are common (11,22), in that Ascaris prevalence and intensity were lower in Vit A+ children. However, to our knowledge, this is the first report where vitamin A supplementation was associated with a delayed rate of reinfection with Ascaris and also the first report where the benefits of vitamin A supplementation on nematode reinfection are detectable in children of normal stature but less so in chronically malnourished children.

Among demographic factors, neither household income nor access to latrines entered any of the regression models as significant determinants of Ascaris reinfection. This was particularly important, given that both are often predictors of Ascaris epg (23) and given that, generally, Vit A+ children had better access to latrines and higher household income than Vit A– children. In contrast, limited mother's education and large households entered as significant predictors of Ascaris epg at 3 and 5 mo, respectively. Limited mothers' education is frequently reported as a risk factor for high intensity Ascaris (24). Where household size is large, the likelihood of contacting Ascaris eggs around the household is also high (25), and thus reinfection would be expected to occur more rapidly in children from larger households. However, over time, the prevalence and intensity of Ascaris in children from smaller households may reach those of children from larger households, thus explaining why the predictive power of household size was not evident at baseline prior to deworming, or at 5 mo after deworming.

Two infection variables entered as significant factors in our regression models. Baseline Ascaris epg had significant predictive power on Ascaris epg 5 mo after deworming, an observation easily explained by the predisposition of certain individuals either to heavy (or light) infection (26) as a result of environmental, behavioral, genetic, immunological, or nutritional factors (26–28). We also observed that older children had higher epg at baseline but not at 3 or 5 mo after deworming. In areas where Ascaris is endemic, intensity increases rapidly with age to a peak in 8- to 10-y–olds, but reinfection rates over the few months following anthelmintic treatment tend to be unaffected by age (28). Thus our findings were consistent with our understanding of the epidemiology of Ascaris.

A low frequency of diarrheal episodes in the month prior to baseline was associated with Ascaris epg at baseline, which was unexpected, given that a recent history of diarrhea had been associated positively with Ascaris infection (29). It has been suggested that geohelminth infections have important protective effects against enteroinvasive infections in young children (30). Moreover, Ascaris is known to induce malabsorption of disaccharides as well as fat (3,4), which would be expected to cause, not protect against, diarrhea (31). However, frequent diarrheal episodes may tend to flush adult worms from the intestinal lumen. We also suggest that the observed link between low frequency of diarrhea and high Ascaris epg could be due to dilution of Ascaris eggs in semiformed stool specimens that were not rejected as "diarrhetic."

The high rate of stunting in the preschool children observed in our study is consistent with a state of chronic malnutrition reported in Panamanian national studies (15). Under such conditions, the physiological response to inadequate quality or quantity of food is reduced linear growth (32). Our results showed that stunting was the strongest nutritional status indicator influencing the impact of vitamin A supplementation on Ascaris infection and reinfection. Moreover, the benefit of vitamin A supplementation in reducing Ascaris reinfection rates persisted longer in children who were not stunted. A recent study associated with the Philippino National Vitamin A Supplementation Program showed that improved retinol levels persisted for a much shorter time in stunted than in nonstunted children (33). Our results could be interpreted similarly, as any protective effect of vitamin A supplementation against reinfection in stunted children was also of very short duration. Socioeconomic factors, normally associated with parasite infection and stunting, did not account for these findings. In contrast, stunted children likely suffer from multiple nutritional deficiencies, and it is possible that vitamin A supplementation alone is insufficient to improve immuno-competence and to increase a child's ability to resist incoming Ascaris eggs. Moreover, low dietary intake of fat and zinc deficiency may interfere with absorption or utilization of the vitamin A provided in the supplements (34). Our results also demonstrated that vitamin A supplementation of children of normal stature not only reduced the existing Ascaris infection, but also reduced reinfection if children were dewormed within 3 mo of supplementation. In contrast, reduced reinfection in stunted children depended on deworming occurring within 6 wk of supplementation. Based on these results, we concluded that the timing of deworming, relative to vitamin A supplementation, is critical to achieving maximum benefit against Ascaris infection, particularly in stunted children.

In the context of public health policy, WHO and UNICEF have recommended that deworming be included in vitamin A supplementation programs delivered every 4–6 mo because of the practical benefits and cost-effectiveness of the combined interventions (7). Our results, emerging from a publicly administered vitamin A supplementation program, demonstrate that, in addition to such practical benefits, there are measurable health advantages to preschool children beyond improving serum retinol concentrations, namely, lower rates of reinfection with Ascaris when supplementation is combined with deworming. Moreover, this integrated approach might lessen the frequency of anthelmintic treatment in areas with endemic parasitosis and, as a consequence, reduce the emergence of drug resistance. Our results suggest that achievement of optimal benefits in high-risk populations with high prevalence of stunting requires that we consider the duration of the benefit of vitamin A supplementation as well as the extent of other coexisting deficiencies. In stunted children, program effectiveness may be enhanced by administering vitamin A capsules every 3–4 mo, by incorporating other micro- or macronutrient supplements in addition to vitamin A, and by coordinating the timing of deworming more closely with supplementation. Future research needs to explore these possibilities. Otherwise, the most vulnerable groups of the population may not receive the full synergistic health benefits of combined interventions with vitamin A and anthelmintics.


   FOOTNOTES
 
1 Supported by the Canadian Institute for Health Research Global Health Planning and Pilot Grant (K.G.K., E.O-B., and M.E.S.) and Canadian International Development Agency Award for Canadians (L.G.P.). Research at the Institute of Parasitology was supported by a regroupement stratégique grant from Le Fonds québécois de la recherche sur la nature et les technologies. Back

2 Author disclosures: L. G. Payne, K. G. Koski, E. Ortega-Barria, and M. E. Scott, no conflicts of interest. Back

5 Abbreviations used: epg, eggs per gram; MOH, Ministry of Health; Vit A+, vitamin A supplemented group; Vit A–, vitamin A unsupplemented group. Back

Manuscript received 23 October 2006. Initial review completed 21 November 2006. Revision accepted 10 March 2007.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

1. Crompton DWT, Montresor A, Nesheim MC, Savioli L. Controlling disease due to helminth infections. Geneva: WHO; 2003.

2. Neumann CG, Gewa C, Bwibo BO. Child nutrition in developing countries. Pediatr Ann. 2004;33:658–74.[Medline]

3. Sivakumar B, Reddy V. Absorption of vitamin A in children with ascariasis. J Trop Med Hyg. 1975;78:114–5.[Medline]

4. Mahalanabis D, Jalan KN, Maitra TK, Agarwal SK. Vitamin A absorption in ascariasis. Am J Clin Nutr. 1976;29:1372–5.[Abstract/Free Full Text]

5. Long KZ, Estrada-Garcia T, Rosado JL, Ignacio Santos J, Haas M, Firestone M, Bhagwat J, Young C, DuPont HC, et al. The effect of vitamin A supplementation on the intestinal immune response in Mexican children is modified by pathogen infections and diarrhea. J Nutr. 2006;136:1365–70.[Abstract/Free Full Text]

6. Ross DA. Recommendations for vitamin A supplementation. J Nutr. 2002;132:2902–6.

7. WHO. Strategy development and monitoring for parasitic diseases and vector control team. How to add deworming to vitamin A distribution. Geneva: WHO/CDS/CPE/PVC/2004.

8. Hagel I, Lynch NR, Di Prisco MC, Perez M, Sanchez JE, Pereyra BN, Soto de Sanabria I. Helminthic infection and anthropometric indicators in children from a tropical slum: Ascaris reinfection after anthelmintic treatment. J Trop Pediatr. 1999;45:215–20.[Medline]

9. Albonico M, Smith PG, Ercole E, Hall A, Chwaya HM, Alawi KS, Savioli L. Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or albendazole in a highly endemic area. Trans R Soc Trop Med Hyg. 1995;89:538–41.[Medline]

10. Albonico M, Bickle Q, Ramsan M, Montresor A, Savioli L, Taylor M. Efficacy of mebendazole and levamisole alone or in combination against intestinal nematode infections after repeated targeted mebendazole treatment in Zanzibar. Bull W H O. 2003;81:343–52.[Medline]

11. Jalal F, Nesheim MC, Agus Z, Sanjur D, Habicht JP. Serum retinol concentrations in children are affected by food sources of beta-carotene, fat intake, and anthelmintic drug treatment. Am J Clin Nutr. 1998;68:623–9.[Abstract]

12. Persson V, Ahmed F, Gebre-Medhin M, Greiner T. Increase in serum beta-carotene following dark green leafy vegetable supplementation in mebendazole-treated school children in Bangladesh. Eur J Clin Nutr. 2001;55:1–9.[Medline]

13. Tanumihardjo SA, Permaesih D, Muherdiyantiningsih, Rustan ME, Rusmil K, Fatah AC, Wilbur S, Muhilal, Karyade D, et al. Vitamin A status of Indonesian children infected with Ascaris lumbricoides after dosing with vitamin A supplements and albendazole. J Nutr. 1996;126:451–7.[Abstract/Free Full Text]

14. Marinho HA, Shrimpton R, Giugliano R, Burini RC. Influence of enteral parasites on the blood vitamin A levels in preschool children orally supplemented with retinol and/or zinc. Eur J Clin Nutr. 1991;45:539–44.[Medline]

15. Ministerio-de-Salud. Estado nutricional de niños preescolares. Panama: Ministerio de Salud; 2000.

16. Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L. Guidelines for the evaluation of soil transmitted helminthiasis and schistosomiasis at community level: a guide for managers of control programs. Geneva: WHO/CTD/SIP/98.1;1998.

17. Gibson RS. Principles of nutritional assessment. New York, Oxford: Oxford University Press; 2005.

18. Erhardt JG, Craft NE, Heinrich F, Biesalski HK. Rapid and simple measurement of retinol in human dried whole blood spots. J Nutr. 2002;132:318–21.[Abstract/Free Full Text]

19. Bennett A, Guyatt H. Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitol Today. 2000;16:71–4.[Medline]

20. Stephensen CB. Vitamin A, infection and immune function. Annu Rev Nutr. 2001;21:167–92.[Medline]

21. Wieringa FT, Dijkhuizen MA, West CE, van der Ven-Jongekrijg J, van der Meer JW, Muhilal. Reduced production of immunoregulatory cytokines in vitamin A- and zinc-deficient Indonesian infants. Eur J Clin Nutr. 2004;58:1498–504.[Medline]

22. Curtale F, Pokhrel RP, Tilden RL, Higashi G. Intestinal helminths and xerophthalmia in Nepal: a case control study. J Trop Pediatr. 1995;41:334–7.[Medline]

23. Holland CV, Taren DL, Crompton DW, Nesheim MC, Sanjur D, Barbeau I, Tucker K, Tiffany J, Rivera G. Intestinal helminthiases in relation to the socioeconomic environment of Panamanian children. Soc Sci Med. 1988;26:209–13.[Medline]

24. Tshikuka JG, Scott ME, Gray-Donald K. Ascaris lumbricoides infection and environmental risk factors in an urban African setting. Ann Trop Med Parasitol. 1995;89:505–14.[Medline]

25. Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RCA. The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Trop Med Int Health. 2004;9:688–701.[Medline]

26. Forrester JE, Scott ME, Bundy DA, Golden MH. Predisposition of individuals and families in Mexico to heavy infection with Ascaris lumbricoides and Trichuris trichiura. Trans Roy Soc Trop Med Hyg. 1990; 84:272–6. Erratum in. Trans R Soc Trop Med Hyg. 1990;84:722.

27. Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M, Grencis RK, Else KJ, Kamgno J, et al. T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect Dis. 2004;190:1804–11.[Medline]

28. Hall A, Anwar KS, Tomkins AM. Intensity of reinfection with Ascaris lumbricoides and its implications for parasite control. Lancet. 1992;339:1253–7.[Medline]

29. Smith H, Dekaminsky R, Niwas S, Soto R, Jolly P. Prevalence and intensity of infections of Ascaris lumbricoides and Trichuris trichiura and associated socio-demographic variables in four rural Honduran communities. Mem Inst Oswaldo Cruz. 2001;96:303–14.[Medline]

30. Cooper PJ, Sandoval C, Chico ME, Griffin GE. Geohelminth infections protect against severe inflammatory diarrhoea in children. Trans R Soc Trop Med Hyg. 2003;97:519–21.[Medline]

31. Bhutta ZA, Ghishan F, Lindley K, Memon IA, Mittal S, Rhoads JM, Commonwealth Association of Paediatric Gastroenterology and Nutrition. Persistent and chronic diarrhea and malabsorption: Working Group Report of the Second World Congress of Pediatric Gastroenterology, Hepatology, and Nutrition. J Pediatr Gastroenterol Nutr. 2004;39: Suppl.2:S711–6.[Medline]

32. Branca F, Ferrari M. Impact of micronutrient deficiencies on growth: the stunting syndrome. Ann Nutr Metab. 2002;46: Suppl 1:8–17.[Medline]

33. Pedro MR, Madriaga JR, Barba CV, Habito RC, Gana AE, Deitchler M, Mason JB. The national vitamin A supplementation program and subclinical vitamin A deficiency among preschool children in the Philippines. Food Nutr Bull. 2004;25:319–29.[Medline]

34. Biesalski HK. Bioavailability of vitamin A. Eur J Clin Nutr. 1997;51: Suppl 1:S71–5.[Medline]





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