The Open Nursing Journal




ISSN: 1874-4346 ― Volume 13, 2019
SYSTEMATIC REVIEW

The Effect of Deworming School Children on Anemia Prevalence: A Systematic Review and Meta-Analysis



Tadele Girum*, Abebaw Wasie
* Department of Public health, college of Medicine and Health Sciences, Wolkite University, Wolkite City, Ethiopia

Abstract

Introduction:

High prevalence of anemia attributable to intestinal parasite infection occurs among children in developing countries. As a result mass treatment of all children with anti-helminthic drugs particularly in school setting is being implemented. There are few studies conducted to assess impact of deworming on anemia prevalence among school children with inconclusive finding. Therefore we aimed to conduct a systematic review on impact assessment of deworming on anemia prevalence or hemoglobin level of school children so that policy makers and other stalk holders could have pooled evidence on the direction to make decision.

Methods:

The review was conducted through a systematic literature search of articles published between 1998 and 2015. Five bibliographic databases and libraries: PubMed/Medline, Global Health Database, Embase, the Cochrane Library, and African Index Medicus were used. After cleaning and sorting, analysis was performed using STATA version 11. The pooled estimate was through a fixed-effects model. Heterogeneity was assessed by the I2 and publication bias through funnel plot.

Results:

Eight studies were retained for final analysis which enrolled a total of 1,005,239 school children. The overall change in the hemoglobin level after deworming was 1.62(95%CI=1.01-2.25) gram/deciliter. There was no difference between the random effect model and the fixed effect model. The prevalence of anemia was markedly changed after the program, particularly in the studies which implemented deworming with hygiene program, co-administration of iron and retinol.

Conclusion and Recommendation:

School based deworming program decreases prevalence of anemia and will contribute to reduction of anemia in the community. Therefore the program should be expanded in all areas and integrated with other child care programs.

Keywords: Deworming, Albendazole, Anemia, Haemoglobin, School health, Parasite infection.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 155
Last Page: 161
Publisher Id: TONURSJ-12-155
DOI: 10.2174/1874434601812010155

Article History:

Received Date: 26/6/2018
Revision Received Date: 1/7/2018
Acceptance Date: 2/07/2018
Electronic publication date: 31/07/2018
Collection year: 2018

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© 2018 Girum and Wasie.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Public health, college of Medicine and Health Sciences, Wolkite University, Wolkite City, Ethiopia, Tel: +251913652268; E-mail: girumtadele@yahoo.com




1. INTRODUCTION

Chronic soil transmitted helminthic infections results in mal-absorption of macro and micronutrients which results in malnutrition like iron deficiency anemia [1WHO. Deworming for health and development: Report of the Third Global Meeting of the Partners for Parasite Control. World health organization, Geneva. 2005.]. Anemia is an overarching public health problem with wide range of consequences. It is the underlying and immediate cause for considerable number of maternal and child morbidity and mortality, loss of productivity among adults, impaired physical and mental development among children [2Gulani A, Nagpal J, Osmond C, Sachdev HPS. Effect of administration of intestinal anthelmintic drugs on haemoglobin: Systematic review of randomised controlled trials. BMJ 2007; 334(7603): 1095.[http://dx.doi.org/10.1136/bmj.39150.510475.AE] [PMID: 17434954] , 3Sachdev H, Gera T, Nestel P. Effect of iron supplementation on physical growth in children: Systematic review of randomised controlled trials. Public Health Nutr 2006; 9(7): 904-20.[http://dx.doi.org/10.1017/PHN2005918] [PMID: 17010257] ]. The causes of anemia are multifactorial including diet, infection and genetics. High prevalence of anemia attributable to intestinal parasite infection occurs among children in developing countries [4Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Savioli L. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: The importance of hookworms. Am J Clin Nutr 1997; 65(1): 153-9.[http://dx.doi.org/10.1093/ajcn/65.1.153] [PMID: 8988928] ].

Worms infect more than one third of the world’s population, with the most intense infections in children and the poor. In the poorest countries, children are likely to be infected from the time they stop breast-feeding, and to be continually infected and re-infected for the rest of their lives [5Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at the community level 1998., 6Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: The great neglected tropical diseases. J Clin Invest 2008; 118(4): 1311-21.[http://dx.doi.org/10.1172/JCI34261] [PMID: 18382743] ]. As a result of the aforementioned fact World Health Organization (WHO) recommends mass treatment of all children with anti-helminthic drugs besides to provision of safe water, improving sanitation and health education [5Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at the community level 1998., 7WHO. Preventive chemotherapy in human helminthiasis. Coordinated use of antihelmintic drugs in control interventions. A manual for health professionals and programme managers. 2006.].

The most commonly used drugs for the deworming of common intestinal worm is albendazole (400 mg) or mebendazole (500 mg). They are administered as a single tablet to all children, regardless of size or age. One pill can cost as little as US$0.02 and only in the most highly infected communities is treatment required more than once a year [8World Health Organization. School Deworming at a glance. 2003.].

The school setting offers an ideal distribution system for public health interventions of many types of health care, including health education, iron supplementation, and treatment or prevention of parasitic infections. The school years are an opportune time to intervene, and interventions must be based on sound epidemiologic understanding of the problem in this age group [4Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Savioli L. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: The importance of hookworms. Am J Clin Nutr 1997; 65(1): 153-9.[http://dx.doi.org/10.1093/ajcn/65.1.153] [PMID: 8988928] ].

The need for program impact (Deworming) evaluation through epidemiologic survey is recommended by World Health Organization [8World Health Organization. School Deworming at a glance. 2003.]. Accordingly there are few studies conducted to assess impact of deworming on anemia prevalence among school children in developing countries with inconclusive finding. Regular anthelmintic delivery (Deworming) has been shown in a number of studies to improve soil transmitted helminthes morbidity indicators, including growth, anemia, cognitive abilities and school attendance [3Sachdev H, Gera T, Nestel P. Effect of iron supplementation on physical growth in children: Systematic review of randomised controlled trials. Public Health Nutr 2006; 9(7): 904-20.[http://dx.doi.org/10.1017/PHN2005918] [PMID: 17010257] , 9Raj SM, Naing NN. Ascariasis, trichuriasis, and growth of schoolchildren in Northeastern Peninsular Malaysia. Southeast Asian J Trop Med Public Health 1998; 29(4): 729-34.[PMID: 10772554] , 10Miguel E, Kremer M. Worms: Identifying impacts on education and health in the presence of treatment externalities. Econometrica 2004; 72.]. There are also other researches with finding of null impact of regular deworming on childhood anemia prevalence [11Davey C, Aiken AM, Hayes RJ, Hargreaves JR. Re-analysis of health and educational impacts of a school-based deworming programme in western Kenya: A statistical replication of a cluster quasi-randomized stepped-wedge trial. Int J Epidemiol 2015; 44(5): 1581-92.[http://dx.doi.org/10.1093/ije/dyv128] [PMID: 26203171] ]. Therefore we aimed to conduct a systematic review on impact assessment of deworming on anemia prevalence or hemoglobin level of school children so that policy makers and other stalk holders could have pooled evidence on the direction program impact to make decision on the prospect of the program.

2. METHODS

2.1. Literature Search Strategy and Eligibility Criteria

This systematic review was conducted through a systematic literature search of articles published between 1998 and 2015 on the effect of deworming school children on anemia prevalence globally. Five bibliographic databases and libraries: PubMed/Medline, Global Health Database, Embase, the Cochrane Library, and African Index Medicus were used. Key words from Medical Subject Headings (MeSHs): Deworming, Albendazole, Mebendazole, Prazequantel, Anemia, Haemoglobin and Heamatocrit were used. In addition the references of each primary researches and reviews were screened and citations were uploaded into an EndNote XI library (EndNote, Carlsbad, CA, USA) and checked for duplications.

Selection was limited to research published in English language that reported the effect of school deworming program in anemia prevalence or hemoglobin level among school age children. Also Studies were eligible regardless of design and setting provided that they fulfill the inclusion criteria. The studies should be conducted on school based deworming program with a follow up period of at least two round administration of any of the medication recommended for deworming programs. The outcome of interest was level of hemoglobin or status of anemia among children who were dewormed one or more rounds. Studies conducted in the same location during the same time period were considered as potential duplicates and therefore excluded from the analysis.

2.2. Data Extraction and Abstraction

All studies we found on the electronic data base search were filtered for potential eligibility and duplications by preformed database and inclusion criteria. Only full studies which were retrieved from the abstracts were reviewed. If needed, and wherever possible, the authors were contacted for clarifications. From each eligible research, the following information was extracted: about author, study participants, studies (study design, cohort size, and setting), Type of medication provided, year of publication, year of study start and end, eligibility criteria, etc. All data were extracted independently and in duplicate using a standardized extraction form. Returned abstracts were reviewed and full texts retrieved if they contained relevant information. Meantime, each selected research was assessed for methodological quality and possibility of bias.

2.3. Data Analysis

After cleaning and sorting the final database was exported into Stata 11.0 for analysis (Stata, College Station, TX, USA) and the Analysis was performed using the ‘metan’ and related functions in STATA version 11 (College Station, TX). Each selected research was reviewed critically and assessed for effect. An outcome of interest was level of hemoglobin or status of anemia among school children who received deworming. Estimates were assessed for each study and standardized mean change with 95% confidence interval was used for level of anemia and its effect assessed for status of anemia. These were calculated with a fixed-effects model. Heterogeneity was assessed by the I2 and Bias was investigated by construction of funnel plots. Results were displayed visually in forest plots.

3. RESULTS

3.1. Studies Included

Initially the search identified 137 citations in the form of abstract, bibliography and full text research from the selected electronic data bases. All citations were transferred to preformed format of endnote and cleaned for duplications and 43 articles were identified for full text review. Of the 43 articles reviewed in full text, 8 articles were analyzed based on the inclusion and exclusion criteria and quality assessment. Among the identified 43 full text studies 35 were removed prior to analysis for different reasons: 4 over lapped with larger studies, 7 were incomplete in one of the inclusion criteria, 13 studies measured other effect of deworming other than anemia and hemoglobin level or measured inconsistently and 11 studies were removed due to program difference, in which they assessed among non-schooled programs (Fig. 1).

Fig. (1)
Flow chart for study search, selection and screening for the review.


3.2. Description of Findings

The 8 full text studies that were retained for final analysis enrolled a total of 1,005,239 school children. Each study enrolled at least 144 school children with in the program and assessed the level of hemoglobin or status of anemia among dewormed and non-dewormed children. Children were received at least one or more round of deworming six months apart and followed for at least a year and the studies were published during the period 1998-2015. Of these studies 5 were cross-sectional and 3 were randomized control trials. Two studies assessed the effect of Mebendazole, 2 studies assessed the effect of Albendazole only and the rest four studies assessed the effect of Albendazole with Prazequantel administration. Four studies were conducted in Asia and four were from Africa. Survey characteristics are described in (Table 1).

Table 1
Characteristics of studies included in the review.


3.3. Pooled Estimates and Tests

Heterogeneity tests showed no significant variations between studies (the weighted sum of squares on a standardized scale was not significantly different compared with expected weighted sum of squares) and I-squared showed that 0% of the observed dispersions are attributed to real rather than spurious variations. Also the funnel plot showed no evidence of publication bias. Therefore the fixed effect model was used to estimate the pooled increase in hemoglobin level after deworming. Based on the estimate, the overall change in the hemoglobin level after deworming was 1.62(95%CI=1.01-2.25) gram/deciliter. There is no difference between the random effect model and the fixed effect model (Fig. 2).

Fig. (2)
Forest plot showing change in hemoglobin level after deworming, weighted according to fixed-effects model.


The minimum change in hemoglobin after deworming of 1.1 (95%CI=0.27-2.47) gram/deciliter was observed in Stoltzfus et al. [17Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 1998; 68(1): 179-86.[http://dx.doi.org/10.1093/ajcn/68.1.179] [PMID: 9665112] ] report, while the maximum changes of 2 gram/deciliter was reported in two studies [14Sufiyan MB, Sabitu K, Mande AT. Evaluation of the effectiveness of deworming and participatory hygiene education strategy in controlling anemia among children aged 6-15 years in Gadagau community, Giwa LGA, Kaduna, Nigeria. Ann Afr Med 2011; 10(1): 6-12.[http://dx.doi.org/10.4103/1596-3519.76561] [PMID: 21311148] , 18Bhoite RM, Iyer UM. Effect of deworming vs Iron-Folic acid supplementation plus deworming on growth, hemoglobin level, and physical work capacity of schoolchildren. Indian Pediatr 2012; 49(8): 659-61.[http://dx.doi.org/10.1007/s13312-012-0129-y] [PMID: 22962239] ]. However the variation was not statistically different between the studies. Besides hemoglobin change in some of the studies the prevalence of anemia was not changed even after repeated cycle of deworming. On the other hand the prevalence of anemia was markedly changed after the program in the studies which implemented deworming with hygiene program, co-administration of iron and retinol (Fig. 2).

4. DISCUSSION

According to this systematic review school-based deworming program significantly increased the level of hemoglobin and reduced the burden of iron deficiency anemia. However the level of change depends on duration of the program or duration of follow up after administration of the drug, frequency of administration and integration of the deworming program with iron, retinol, nutrition and hygiene programs [12Kinung’hi SM, Magnussen P, Kishamawe C, Todd J, Vennervald BJ. The impact of anthelmintic treatment intervention on malaria infection and anaemia in school and preschool children in Magu district, Tanzania: an open label randomised intervention trial. BMC Infect Dis 2015; 15: 136.[http://dx.doi.org/10.1186/s12879-015-0864-5] [PMID: 25887977] , 14Sufiyan MB, Sabitu K, Mande AT. Evaluation of the effectiveness of deworming and participatory hygiene education strategy in controlling anemia among children aged 6-15 years in Gadagau community, Giwa LGA, Kaduna, Nigeria. Ann Afr Med 2011; 10(1): 6-12.[http://dx.doi.org/10.4103/1596-3519.76561] [PMID: 21311148] , 16Guyatt HL, Brooker S, Kihamia CM, Hall A, Bundy DAP. Evaluation of efficacy of school-based anthelmintic treatments against anaemia in children in the United Republic of Tanzania. Bull World Health Organ 2001; 79(8): 695-703.[PMID: 11545325] -18Bhoite RM, Iyer UM. Effect of deworming vs Iron-Folic acid supplementation plus deworming on growth, hemoglobin level, and physical work capacity of schoolchildren. Indian Pediatr 2012; 49(8): 659-61.[http://dx.doi.org/10.1007/s13312-012-0129-y] [PMID: 22962239] ]. In all of the studies included in this review deworming caused improvements in iron status which is measured by protoporphyrin, a measure of iron-deficient erythropoiesis, and serum ferritin, a measure of iron stores and hemoglobin level. This is in line to previous reports [2Gulani A, Nagpal J, Osmond C, Sachdev HPS. Effect of administration of intestinal anthelmintic drugs on haemoglobin: Systematic review of randomised controlled trials. BMJ 2007; 334(7603): 1095.[http://dx.doi.org/10.1136/bmj.39150.510475.AE] [PMID: 17434954] -4Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Savioli L. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: The importance of hookworms. Am J Clin Nutr 1997; 65(1): 153-9.[http://dx.doi.org/10.1093/ajcn/65.1.153] [PMID: 8988928] , 9Raj SM, Naing NN. Ascariasis, trichuriasis, and growth of schoolchildren in Northeastern Peninsular Malaysia. Southeast Asian J Trop Med Public Health 1998; 29(4): 729-34.[PMID: 10772554] ]. It is also long been known that deworming prevents hook worm infection which is one of the major cause of iron loss in children and in turn prevents anemia [5Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at the community level 1998., 7WHO. Preventive chemotherapy in human helminthiasis. Coordinated use of antihelmintic drugs in control interventions. A manual for health professionals and programme managers. 2006., 8World Health Organization. School Deworming at a glance. 2003.]

In studies which have longer follow up period and studies which integrated deworming program with iron supplementation the level of change in hemoglobin and reduction in the prevalence of anemia was higher. Among the studies included in the review Stoltzfus et al. [17Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 1998; 68(1): 179-86.[http://dx.doi.org/10.1093/ajcn/68.1.179] [PMID: 9665112] ] indicated that change in hemoglobin level and prevalence of anemia was observed on children who received two-three times a year. Similarly Bhoite et al. [18Bhoite RM, Iyer UM. Effect of deworming vs Iron-Folic acid supplementation plus deworming on growth, hemoglobin level, and physical work capacity of schoolchildren. Indian Pediatr 2012; 49(8): 659-61.[http://dx.doi.org/10.1007/s13312-012-0129-y] [PMID: 22962239] ] and Sufiya et al. [14Sufiyan MB, Sabitu K, Mande AT. Evaluation of the effectiveness of deworming and participatory hygiene education strategy in controlling anemia among children aged 6-15 years in Gadagau community, Giwa LGA, Kaduna, Nigeria. Ann Afr Med 2011; 10(1): 6-12.[http://dx.doi.org/10.4103/1596-3519.76561] [PMID: 21311148] ] reported that significant change in hemoglobin level was observed only when deworming was integrated with iron supplementation and hygiene education respectively. In line to our review significant increases in hemoglobin concentration were reported when deworming was provided along with iron supplementation among school children in south Africa [20Kruger M, Badenhorst CJ, Mansvelt EPG, Laubscher JA, Benade AJS. Effects of iron fortification in a school feeding scheme and anthelmintic therapy on the iron status and growth of six-to eightyear-old schoolchildren. Food Nutr Bull 1996; 17: 11-21.], and India [21Working Group on Fortification of Salt with Iron. Use of common salt fortified with iron in the control and prevention of anemia--a collaborative study. Report of the Working Group on Fortification of Salt with Iron. Am J Clin Nutr 1982; 35(6): 1442-51.[http://dx.doi.org/10.1093/ajcn/35.6.1442] [PMID: 7081125] ], and nutritional supplementation in Papua New Guinea [22Shield JM, Vaterlaws AL, Kimber RJ, et al. The relationship of hookworm infection, anaemia and iron status in a Papua New Guinea highland population and the response to treatment with iron and mebendazole. P N G Med J 1981; 24(1): 19-34.[PMID: 6945770] ].

However in some studies [13Awasthi S, Peto R, Read S, Richards SM, Pande V, Bundy D. Population deworming every 6 months with albendazole in 1 million pre-school children in North India: DEVTA, a cluster-randomised trial. Lancet 2013; 381(9876): 1478-86.[http://dx.doi.org/10.1016/S0140-6736(12)62126-6] [PMID: 23498850] ] despite improvements in iron status, the deworming program had no detectable effects on average hemoglobin concentrations or the prevalence of anemia. This may be due to the fact that change in the level of hemoglobin and prevalence of anemia takes a longer duration (12-15 months) after the child was dewormed [23Tee E, Kandiah M, Awin N, Chong S, et al. School administered weekly iron folate supplements improve hemoglobin and ferritin concentrations in Malaysian adolescent girls. Am J Clin Nutr 1999; 69: 1249 -56.[http://dx.doi.org/10.1093/ajcn/69.6.1249] ]. As a result in some studies significant difference was not observed, when they have shorter follow up period. In line to this in another study, improvement in the hemoglobin level was not detected until 10 months of deworming intervention [18Bhoite RM, Iyer UM. Effect of deworming vs Iron-Folic acid supplementation plus deworming on growth, hemoglobin level, and physical work capacity of schoolchildren. Indian Pediatr 2012; 49(8): 659-61.[http://dx.doi.org/10.1007/s13312-012-0129-y] [PMID: 22962239] , 24Martorell R, Scrimshaw NS. The effects of improved nutrition in early childhood: The INCAP follow-up study. J Nutr 1995; 125: 4S.[PMID: 7722705] ]. It is expected that in our review too the positive impact of the study could be seen in the later years.

The primary aim of deworming is to prevent iron loss ascribed to hook worm infection. Therefore after deworming nutritional improvement and iron supplementation programs are compulsory for prevention of anemia [5Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at the community level 1998.-7WHO. Preventive chemotherapy in human helminthiasis. Coordinated use of antihelmintic drugs in control interventions. A manual for health professionals and programme managers. 2006.]. Because deworming acts primarily by decreasing iron loss, in populations with limited absorbable dietary iron the expected effect from deworming would be to halt or slow the decline in iron status associated with hookworm infection.

In this regard, when children are not getting enough iron even though they are dewormed the hemoglobin level may not be changed. Particularly those children who are malnourished, absorption of iron will be reduced and change in hemoglobin may not be attained. On the other hand iron-specific indicators, ferritin and protoporphyrin which have a faster turnaround changed almost in all studies reviewed. Therefore, as observed in some other studies [17Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 1998; 68(1): 179-86.[http://dx.doi.org/10.1093/ajcn/68.1.179] [PMID: 9665112] , 18Bhoite RM, Iyer UM. Effect of deworming vs Iron-Folic acid supplementation plus deworming on growth, hemoglobin level, and physical work capacity of schoolchildren. Indian Pediatr 2012; 49(8): 659-61.[http://dx.doi.org/10.1007/s13312-012-0129-y] [PMID: 22962239] ] integration of deworming program with iron supplementation and nutrition programs yield better response.

CONCLUSION AND RECOMMENDATION

School based deworming program (administration of intestinal anti-helminthic drugs) results in increase in hemoglobin level and decreases prevalence of anemia among school children. Thus school based intervention will contribute to reduction of anemia in the community. Better outcome was observed among programs which integrated deworming with iron and nutrition supplementation programs. Therefore school based deworming programs should be expanded in all areas and should be integrated with other child care programs.

AVAILABILITY OF DATA AND MATERIALS

Please contact author for data requests.

AUTHOR INFORMATION

TG: is Bsc/public health, MPH in Epidemiology and Biostatistics, Lecturer at Department of Public health, College of Medicine and Health Sciences, Wolkite University, Wolkite, Ethiopia

AW: is Bsc/public health, MPH in Reproductive health, Lecturer at Department of Public health, College of Medicine and Health Sciences, Wolkite University, Wolkite, Ethiopia

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.

HUMAN AND ANIMAL RIGHTS

No animals/humans were used for studies that are the basis of this review.

FUNDING

Not applicable

AUTHORS CONTRIBUTIONS

Not applicable

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

For all authors who provided us information whenever we contacted them.

REFERENCES

[1] WHO. Deworming for health and development: Report of the Third Global Meeting of the Partners for Parasite Control. World health organization, Geneva. 2005.
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[3] Sachdev H, Gera T, Nestel P. Effect of iron supplementation on physical growth in children: Systematic review of randomised controlled trials. Public Health Nutr 2006; 9(7): 904-20.[http://dx.doi.org/10.1017/PHN2005918] [PMID: 17010257]
[4] Stoltzfus RJ, Chwaya HM, Tielsch JM, Schulze KJ, Albonico M, Savioli L. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: The importance of hookworms. Am J Clin Nutr 1997; 65(1): 153-9.[http://dx.doi.org/10.1093/ajcn/65.1.153] [PMID: 8988928]
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[14] Sufiyan MB, Sabitu K, Mande AT. Evaluation of the effectiveness of deworming and participatory hygiene education strategy in controlling anemia among children aged 6-15 years in Gadagau community, Giwa LGA, Kaduna, Nigeria. Ann Afr Med 2011; 10(1): 6-12.[http://dx.doi.org/10.4103/1596-3519.76561] [PMID: 21311148]
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[17] Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 1998; 68(1): 179-86.[http://dx.doi.org/10.1093/ajcn/68.1.179] [PMID: 9665112]
[18] Bhoite RM, Iyer UM. Effect of deworming vs Iron-Folic acid supplementation plus deworming on growth, hemoglobin level, and physical work capacity of schoolchildren. Indian Pediatr 2012; 49(8): 659-61.[http://dx.doi.org/10.1007/s13312-012-0129-y] [PMID: 22962239]
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Endorsements



"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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