Advertisement
  • Loading metrics

Soil-transmitted helminth infections and nutritional indices among Filipino schoolchildren

  • Mary Lorraine S. Mationg ,

    Roles Formal analysis, Investigation, Project administration, Writing – original draft, Writing – review & editing

    Mary.Mationg@anu.edu.au (MLSM); darren.gray@anu.edu.au (DJG)

    Affiliations Research School of Population Heath, The Australian National University, Canberra, Australia, Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Gail M. Williams,

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Supervision, Writing – review & editing

    Affiliation School of Public Health, University of Queensland, Brisbane, Australia

  • Veronica L. Tallo,

    Roles Funding acquisition, Investigation, Project administration, Supervision, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Remigio M. Olveda †,

    † Deceased.

    Roles Funding acquisition, Investigation, Project administration, Supervision

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Eindra Aung,

    Roles Investigation, Project administration, Writing – review & editing

    Affiliations Research School of Population Heath, The Australian National University, Canberra, Australia, St Vincent’s Clinical School, University of New South Wales, Sydney, Australia

  • Portia Alday,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Mark Donald Reñosa,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Chona Mae Daga,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Jhoys Landicho,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Maria Paz Demonteverde,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Eunice Diane Santos,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Thea Andrea Bravo,

    Roles Investigation, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

  • Franziska Angly Bieri,

    Roles Investigation, Writing – review & editing

    Affiliation Research School of Population Heath, The Australian National University, Canberra, Australia

  • Yuesheng Li,

    Roles Funding acquisition, Investigation, Writing – review & editing

    Affiliations Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia, Hunan Institute of Parasitic Diseases, World Health Organization Collaborating Centre for Research and Control on Schistosomiasis in Lake Region, Yueyang, China

  • Archie C. A. Clements,

    Roles Funding acquisition, Investigation, Writing – review & editing

    Affiliation Faculty of Health Sciences, Curtin University, Perth, Australia

  • Peter Steinmann,

    Roles Conceptualization, Funding acquisition, Writing – review & editing

    Affiliations Swiss Tropical and Public Health Institute, Basel, Switzerland, University of Basel, Basel, Switzerland

  • Kate Halton,

    Roles Funding acquisition, Writing – review & editing

    Affiliation School of Public Health and Social Work, Queensland University of Technology, Brisbane, Australia

  • Donald E. Stewart,

    Roles Funding acquisition, Writing – review & editing

    Affiliations Research School of Population Heath, The Australian National University, Canberra, Australia, School of Medicine, Griffith University, Brisbane, Australia

  • Donald P. McManus ,

    Roles Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing – review & editing

    ‡ These authors are joint senior authors on this work.

    Affiliation Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia

  •  [ ... ],
  • Darren J. Gray

    Roles Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing – review & editing

    Mary.Mationg@anu.edu.au (MLSM); darren.gray@anu.edu.au (DJG)

    ‡ These authors are joint senior authors on this work.

    Affiliation Research School of Population Heath, The Australian National University, Canberra, Australia

  • [ view all ]
  • [ view less ]

Abstract

Background

Soil-transmitted helminth (STH) infections are still prevalent among schoolchildren in the Philippines. We evaluated the risk factors associated with STH and the relationship between STH and nutritional indices among schoolchildren aged 9–10 years in Laguna province, the Philippines.

Methods

We used the baseline data from 40 schools enrolled in a randomised controlled trial of the Magic Glasses Philippines health education package. Data on demographic and socio-economic variables, and STH related knowledge, attitudes and practices, were obtained through a questionnaire. Stool samples were collected and assessed for STH egg presence using the Kato-Katz technique. Haemoglobin levels and height and weight of study participants were also determined. The generalized estimating equations approach was used to construct logistic regression models to assess STH-associated risk factors, and the association between any STH infection and anaemia, child stunting, wasting and being underweight. The trial is registered with the Australian New Zealand Clinical Trials Registry (ACTRN12616000508471).

Findings

Among 1,689 schoolchildren, the prevalence of any STH was 23%. The prevalence of anaemia, stunting, being underweight and wasting was 13%, 20.2%, 19% and 9.5%, respectively. Age, socio-economic status, rural/urban classification of schools and knowledge of STH were significant risk factors for acquiring a STH infection. Moreover, infections with any STH were significantly associated with stunting (P = <0.001) and being underweight (P = <0.003), but not wasting (P = 0.375) or anaemia (P = 0.462) after controlling for confounding covariates.

Conclusion

The study findings emphasise the need for sustainable deworming in tandem with other measures such as the provision of health education, improvements in sanitation and hygiene, and nutritional programs in order to control STH infections and improve morbidity outcomes in schoolchildren.

Trial registration

Australian New Zealand Clinical Trials Registry (ACTRN12616000508471).

Author summary

Soil-transmitted helminth (STH) infections continue to be high among schoolchildren in the Philippines despite the conduct of semi-annual nationwide school-based mass drug administration (MDA) program more than a decade ago. In this cross-sectional survey, we assess the prevalence of STH, the risk factors associated with infection, and the impact of STH on nutritional indices among schoolchildren in Laguna province, the Philippines. Our results show that STH prevalence (23%) remains above the World Health Organization (WHO) target of < 20% for morbidity control. The prevalences of stunting (20.2%), being underweight (19%) or wasting (9.5%) are high and are still regarded as public health problems according to WHO criteria, but low anaemia prevalence (13%) was observed. Age, socio-economic status, rural/urban classification of schools and knowledge of STH were significant risk factors for STH infections. Moreover, infections with STH were significantly associated with stunting and being underweight but not wasting or anaemia after controlling for key confounders. Sustainable deworming in tandem with other measures such as the provision of health education, improvements in sanitation and hygiene, and nutritional programs, are needed to control intestinal worm infections and improve morbidity outcomes in schoolchildren.

Introduction

Soil-transmitted helminth (STH) infections are the most prevalent of the neglected tropical diseases (NTD). They infect more than one billion individuals world-wide [1]. In 2021, the World Health Organization (WHO) declared ambitious targets to reduce the burden of STH by eliminating them as a public health problem by 2030 [2]. Morbidity due to STH has been accounted to range from 1.97–3.3 million disability-adjusted life years (DALYs) [3,4]; school-aged children usually experience the highest burden [5]. Morbidities associated with STH in children include malnutrition, impaired growth, anaemia, and cognitive and educational deficits [6,7].

In the Philippines, STH are highly prevalent and major health problem, particularly in schoolchildren [8]. STH prevalence reported from several studies across the country range from 33.8–75.9% [914]. This is despite the implementation of a semi-annual nationwide school-based mass drug administration (MDA) program that was initiated more than a decade ago [15,16]. Notwithstanding the considerable efforts undertaken in the Philippines to control STH through regular school-based MDA, the persistence of STH requires careful assessment of the risk factors associated with infection and the morbidity burden.

Data from a recent (2018) Philippines National Nutrition Survey by the Food and Nutrition Research Institute of the Department of Science and Technology (FNRIDOST) indicated that stunting (24.5%) and being underweight (25%) remain highly prevalent among 6–10 year old schoolchildren, while the prevalence of wasting was 7.6% [17]. Furthermore, the prevalence of anaemia has also increased, affecting some 23.5% of six-year old children [17], translating into a moderate public health problem based on WHO criteria [18].

There are several reports from the Philippines on the factors associated with malnutrition in children [1923] but relatively few have described the impact of STH [13,2426]. Furthermore, previous studies correlating STH infections with anaemia are conflicting [2730]. As the impact of STH on children’s health has not been extensively reported in the Philippines, studies assessing STH-associated morbidity in children are therefore needed to effectively monitor the success of STH control program in country. The present study was undertaken to determine STH prevalence, the risk factors associated with infection, and the impact of STH on nutritional indices among schoolchildren in Laguna province, the Philippines.

Methods

Ethics statement

Ethical clearance was obtained from the Research Institute for Tropical Medicine (RITM) Institutional Review Board (approval number 2013–16), the Philippines, QIMR Berghofer Medical Research Institute Human Ethics Committee (approval number: P1271), Australia, and the Australian National University Human Ethics Committee (approval number: 2014/356). Permission to undertake the study was obtained from the Philippines Department of Education (DepEd) prior to the start of the study. Written informed consent was obtained from parents and guardians of children. Written assent was also obtained from students who agreed to participate. Parasitological and anaemia results were communicated to all parents at the end of the survey, with a recommendation to seek treatment from local health centres.

Study setting, design and participants

This study was conducted as part of the baseline assessment for a cluster randomised controlled trial (RCT) of “The Magic Glasses Philippines”. The trial aimed to determine the impact and generalizability of the school-based health education package for the prevention of STH in Laguna province [31,32]. Laguna is located on the Island of Luzon, in the Calabarzon Region of the Philippines, with 3.3 million population as of the last census conducted in 2020. It is also considered as the 3rd populous and densest province in the Philippines [33]. Due to the high STH infections (averages ~33%), as confirmed by our pilot survey in 2015 [11], we have selected this area as the study site for the main RCT. The 40 schools included in the study were selected using a spatial sampling technique and according to the inclusion criteria of minimum three kilometres distance from each other. Further details of the design of the RCT, the study setting and procedures are available in the published study protocol [31]. The study baseline survey was carried out (June and July 2016) on schoolchildren aged 9–10 years (Grade 4) in 40 selected schools.

The sample size for present study was bound by the sample size calculation for the main RCT. This was designed to have 80% power to detect the intervention effect, using an intervention efficacy of 30% [18]. Calculations assumed an infection prevalence of 18% and a design effect of 1.5 to account for the cluster effect, and a predicted annual 10% loss-to-follow-up. The sample size calculation determined the requirement of 20 clusters for each study group (40 in total), corresponding to 1,520 study participants (assuming 38 participants per cluster).

Study procedures

KAP questionnaire.

All study participants completed a questionnaire to collect data on demographics, and knowledge, attitude and practices (KAP) about STH infection at trial baseline [31]. Full details of the questionnaires and KAP survey procedures are provided in the published study protocol [31]. In brief, the KAP questionnaire included multiple-choice and open-ended questions on demographics, health characteristics, medical history, and previous health education; knowledge about intestinal worms, how they are transmitted, and the symptoms and treatment of STH infection; the student’s attitude toward STH; self-reported hygiene practices in relation to hand washing, handling of food, using the toilet, and wearing of shoes. The questionnaire was developed in English, translated to Tagalog and back-translated into English to ensure accuracy. It was also pre-tested in two schools outside the RCT trial area.

The questionnaire was administered to the children by two research staff members. The instructions and questions in the questionnaire are read one-by-one to the children in front of the class by the first staff whereas the other moved around the room to check whether the children were able to follow the instructions and to ensure that each question was answered. The research staff had undergone a one-week training on data collection procedures including the administration of the KAP questionnaire before the start of the survey [31].

The data on the household characteristics associated to household water source and household assets were collected in the first trial follow-up KAP survey and we assumed that the status of the household characteristics did not change in the 5 months following the baseline survey.

Parasitological examination.

Schoolchildren were asked to provide two stool samples over a period of four collection days to the research staff at the school [31]. From each sample, triplicate Kato-Katz (KK) thick smears (41.7 mg of stool/smear) were prepared at the school site within two hours after collection and these were all examined the same day [34]. Eggs were counted for all STH species to record prevalence and infection intensity (eggs per gram of faeces; EPG). Intensity of infection for each species was interpreted as light, moderate or heavy based on WHO criteria [35]. Prevalence of STH was defined as the presence of at least one STH species or genus (i.e., A. lumbricoides and/or T. trichiura and/or hookworm). For quality control, 10% of all slides were randomly selected and re-examined by a reference microscopist on each collection day.

Nutritional status assessment.

All participating children underwent a single measurement at baseline of height (to nearest 0.1 cm) using a height scale chart (paper beam chart) and weight (to nearest 0.1 kg) using a calibrated digital weighing scale (Tanita HD-383, Tanita Corporation, Japan). Indicators for malnutrition included height-for-age Z-score (HAZ) to assess stunting, body mass index (BMI)-for-age Z-score (BAZ) to assess wasting, and weight-for-age Z-score (WAZ) (children aged <10 years only) to assess underweight. The calculations were done using the SAS macros for 2007 WHO Child Growth Standards for school-aged children and adolescents [36]. Each of these continuous outcomes was categorised, with individuals classified as stunted, underweight or wasted if HAZ, WAZ and BAZ, respectively, were more than two standard deviations below the WHO growth reference values [37].

Haemoglobin concentration assessment.

Finger-prick blood samples were collected from participating children using a portable haemoglobin analyser (HemoCue Hb 301 System, HemoCue Sweden). The haemoglobin level was classified according to the WHO definition of anaemia severity (i.e., non-anaemic, mild, moderate and severe) [38]. However, due to the skewed distribution of those categorized as having mild, moderate or severe anaemia, anaemia status was re-categorized as a binary variable (defined as anaemic/non-anaemic using the cut-off set by WHO [38]) and used as a primary outcome.

Data analysis

Analyses to determine the association between STH infections and nutritional indices (i.e., stunting, wasting, underweight and anaemia) were undertaken using the baseline cross-sectional data from the 40 schools enrolled in the Magic Glasses Philippines RCT. The analyses included study participants with complete data on KAP, at least one stool sample, blood sample, height and weight at baseline, and with a first follow-up KAP at 6 months.

To establish the socio-economic status (SES) of the study participants, we used a household-based asset approach [39]. Employing principal component analysis (PCA), a household wealth index variable was constructed from nine indicators: cement or tile floor material, access to electricity, having a radio, television set, refrigerator, cell phone, bicycle, motorcycle or jeep, or a truck. Children were asked about the presence of each indicator in the household. The factor scores from the first principal component were used as a measure of SES [39]. The first principal component explained 21.7% of the total variability. Variables such as the type of toilet used and the source of available drinking water were excluded from the PCA analysis as they were considered risk factors for STH infection in their own right.

For the KAP questionnaire, each correct answer for the knowledge and attitude components carried a score of one mark, an incorrect answer received a minus one mark and a “don’t know” answer was scored zero. In the case of the practices component, “Never” was scored zero, while “Some of the time”, “Most of the time” and “Always” were scored as “1”, “2” and “3”, respectively. “Always” shows maximum frequency for an event, and therefore was assigned the highest score. The overall scores calculated for the knowledge, attitude and practice components in the KAP questionnaire were 31, 7 and 29, respectively. The respondents’ overall knowledge level and practice securing a score of 20 or more were categorized as having good, 11–19 scores as an average, and ≤10 scores as poor. For overall attitude score, respondents with a score of 6 or more were categorized as having a good attitude, 4–5 scores as an average attitude, and ≤3 scores as a poor attitude. Meanwhile, for the knowledge sub-component scores (i.e., overall knowledge score on STH transmission and signs and symptoms), respondents with a score of 5–6 were categorized as having good, 3–4 scores as an average, and ≤2 scores as a poor. For overall knowledge score on STH prevention, respondents with a score of 7–9 were categorized as having good, 4–6 scores as an average, and ≤3 scores as poor.

A generalized estimating equations (GEE) approach was used to construct logistic regression models to account for possible clustering at the school level. Logistic regression models were constructed to assess the following: 1) predictors of STH infections; 2) the association between stunting, being underweight and wasting odds, and STH infection status adjusting for age, SES, anaemia and rural/urban classification of schools (according to the Philippines Statistical Authority (PSA) rural/urban classification of villages where the schools were located); and 3) the association between anaemia and STH infection status adjusting for age, sex, SES and rural/urban classification of each school. For the model predicting the risk factors for STH infections, univariable regression was undertaken for each of the risk factors, with inclusion in the multivariable model if they had P<0.2 and then removed iteratively until only the variables significant at P<0.05 remained in the final model. For model assessing the associations between STH infection and nutritional indices; and between STH infection and anaemia, all potential confounders regardless of their significance in the univariate analysis were forced in the final model. For models of stunting, being underweight and wasting, anaemia was added because of its importance as a potential confounder.

All data management and analyses used SAS Proprietary Software 9.4 (TS1M3) [Copyright 2002–2012 by SAS Institute Inc., Cary, NC, USA, Licensed to AUSTRALIAN NATIONAL UNIVERSITY–EAS, Site 10004431].

Results

General characteristics of the study population

At baseline, 3,832 students from the 40 targeted schools consented to participate in the study. Of those providing consent, 1,774 had complete data on baseline KAP, at least one stool sample, finger-prick blood sample, and height and weight measurements. Of these 1,774 students, 1,689 (95%) had matching KAP data at first follow up and were included in the analysis.

More than half of the participating schoolchildren were female (54.1%); the majority (89.2%) were aged 7–9 years (median age of study participants at enrolment was 9 years; interquartile range [IQR], 8–9 years). The majority (73.2%) of the students attended urban schools. Almost half (46.5%) of the respondents reported sourcing their drinking water from a piped water source and 71.9% reported using a pour-flush or water-sealed toilet (Table 1).

thumbnail
Table 1. Demographic and household characteristics of schoolchildren in Laguna Province, Philippines (n = 1,689).

https://doi.org/10.1371/journal.pntd.0010008.t001

Prevalence of STH and nutritional characteristics

Of the 1,689 schoolchildren included, 389 (23%) were infected with at least one STH species, with the prevalence for A. lumbricoides, T. trichiura and hookworm being 15.9%, 13.3%, and 0.12% respectively. Among these, 63.2%, 94.2% and 100% of the infected children had light intensity burdens of A. lumbricoides, T. trichiura and hookworm, respectively. Prevalences of stunting, being underweight or wasting were 20.2%, 19.0% and 9.5% respectively. Only 13.0% of the study population suffered from anaemia, with the majority of these (11.1%) being mildly anaemic, and 1.9% were severely anaemic (Table 2).

thumbnail
Table 2. STH prevalence and nutritional characteristics of schoolchildren in Laguna Province, the Philippines (n = 1,689).

https://doi.org/10.1371/journal.pntd.0010008.t002

Knowledge of STH

Sixty-four percent of the schoolchildren in the study acknowledged having previously heard of intestinal worms; A. lumbricoides or roundworms was heard by 53.2% of the schoolchildren, while 44.5% and 15.6% knew about T. trichiura or whipworms and hookworm, respectively. The majority indicated nurse/doctor (53.0%), television (49.5%), parents (44.9%) or school (41.4%) as the source of this information. About 67.1%, 47.4% and 43.8% of children were categorized as having poor knowledge of STH signs and symptoms, STH transmission and prevention, respectively (Table 3).

thumbnail
Table 3. Knowledge on STH transmission, signs and symptoms of infection and preventive measures.

https://doi.org/10.1371/journal.pntd.0010008.t003

The great majority (93.3%) of participating schoolchildren believed that STH infections are treatable. When asked where they should receive treatment, a majority answered health centre (78.90%) or hospital (70.5%), while a small proportion answered school (7.0%), parent (7.2%) or traditional healer (6.0%). A majority (63.4%) considered that STH treatment prevented reinfection. Overall the STH knowledge score indicated that more than half (58.5%) of the schoolchildren had an average knowledge of intestinal worms (Table 3).

Attitude and practices of schoolchildren towards STH infection

The KAP questionnaire further revealed that the majority (86%) of the schoolchildren believed that they had a chance of STH infection; of these, 36.8% considered they had a medium chance of acquiring the infection. The majority (76.7%) reported that they would worry if they became infected. However, 42.5% of participants did not consider that STH infection would prevent them from attending school. Furthermore, 85.6% reported they were able to wash their hands after toilet use at school. Overall, 46.2% of the schoolchildren had an average attitude score regarding STH infection (see S1 Table for additional information).

In relation to reported STH prevention practices, 81.9% indicated they always wore slippers outside their home, wore slippers inside the house (43.5%) and wore shoes at school (79.8%). Most of the children reported that they always defecated in their home latrine (86.1%) while a small proportion indicated they used a public/shared latrine (4.1%), the field (2.7%), and river or canal (1.7%). The majority (74%) indicated they always washed hands after toilet use; and 81.9% indicated they always used soap when washing. Similarly, the majority (87.8%) indicated they always washed their hands before eating with 80.2% always using soap. The majority also indicated the practice of washing fruits before eating (88.3%), and covering leftover food (81.8%) at all times. In general, 91.1% of the study participants were categorized as having good self-reported practices towards STH prevention (see S1 Table for additional information).

Factors associated with STH infection

Multivariate logistic regression using GEE modelling showed that increasing age (age as a continuous variable) was significantly associated with STH infection (Adjusted Odds Ratio (AOR: 1.5; 95% Confidence Interval [CI]: 1.3─1.8; P = <0.001). The SES score was also found associated with an increased odds of STH infection (AOR: 1.2; 95% CI: 1.1–1.3; P = 0.001). However, unexpectedly, children located in rural schools (AOR: 0.7; 95% CI: 0.5–0.9; P = 0.016) were significantly less likely to have a STH infection compared with urban schools. Moreover, children with poor (AOR: 1.2; 95% CI: 1.0–1.6; P = 0.185) and average knowledge of STH (AOR: 1.2; 95% CI: 1.1–1.5; P = 0.013) were more likely to have STH infection, compared with students with good STH knowledge. There was no significant association of STH infection with sex, main source of drinking water, type of toilet, STH attitude score or practice (Table 4).

thumbnail
Table 4. Univariate and multivariate analysis assessing risk factors associated with any STH infection among schoolchildren in Laguna Province, the Philippines.

https://doi.org/10.1371/journal.pntd.0010008.t004

Association between STH infection and nutritional indicators

Multivariate GEE regression modelling was used separately to assess the relationships between STH infection status and stunting; being underweight; and wasting (Table 5). Stunting (AOR: 1.3; 95% CI: 1.1–1.6; P = <0.001) and being underweight (AOR: 1.7; 95% CI: 1.2–2.3; P = 0.003), but not wasting (AOR: 1.2; 95% CI: 0.8–1.7; P = 0.375), were significantly associated with STH infection after adjusting for age, sex, SES, rural/urban classification of schools, presence of anaemia and within school clustering. Additionally, the multivariate GEE regression model was used to assess the relationship between STH and anaemia but no significant association (AOR: 1.1; 95% CI: 0.9–1.7; P = 0.462) was evident after controlling for age, sex, SES, rural/urban classification of schools and within school clustering (Table 6).

thumbnail
Table 5. Associations between any STH and nutritional indices among schoolchildren in Laguna Province, the Philippines based on a generalized estimating equations (GEE) logistic regression model.

https://doi.org/10.1371/journal.pntd.0010008.t005

thumbnail
Table 6. Associations between any STH and anaemia among schoolchildren in Laguna Province, the Philippines based on a generalized estimating equations (GEE) logistic regression model.

https://doi.org/10.1371/journal.pntd.0010008.t006

Discussion

The results of this study showed that the overall prevalence of STH infection (23%) in the Laguna province study population remains above the WHO target of <20% for morbidity control. The true prevalence is likely to be higher due to the use of KK, which is known to decrease in sensitivity as prevalence and infection intensity decrease [11]. Nevertheless, the current prevalence estimate indicates that STH continues to be a public health problem among schoolchildren in this area. The most prevalent species present was A. lumbricoides (15.9%) followed by T. trichuris (13.3%), while a very small percentage of hookworm infections (0.12%) was recorded; this was not surprising given the low hookworm prevalence (6.8%) in Laguna province previously reported [11]. The majority of the schoolchildren had light intensity A. lumbricoides, T. trichiura infections or hookworm. The low infection intensity is likely attributable to the routine semi-annual deworming programme implemented in the study area.

Our KAP survey revealed that 64% of the schoolchildren claimed to be aware of intestinal worms, but follow-up questions demonstrated low levels of knowledge in some aspects. Misconceptions related to STH transmission, signs and symptoms, preventive measures and treatment among study participants were evident, indicating a lack of health education on STH. The majority of schoolchildren demonstrated an average attitude towards STH infection. This suggests the need for appropriate preventive programs to increase not only the knowledge of schoolchildren but also to improve their attitude towards STH. Although the majority of the study participants were categorized as having good practice regarding STH prevention, it was notable that a small proportion indicated they always defecated in the field or in a bush (3%) and in the river or canal (2%), indicating another gap in sanitary/hygienic practices. Of those who reported practicing open defecation, the majority (96%) recorded having a latrine/toilet at home. However, as we did not collect information on the functionality of sanitary facilities at home, it may be possible that not all children were able or willing to use a latrine or toilet in the home or at school.

In terms of potential risk factors for STH infection, our study showed that the risk of STH infection increased with age, emphasizing the importance of preventive chemotherapy in children during their primary school years, given that the peak prevalence and intensity occur during this period [41]. SES score was also found to be strongly associated with STH infections. In general, low SES reflects poverty which limits an individual’s access to safe, clean and adequate water supply and improved sanitation, and this results in an increased likelihood of transmission and maintenance of intestinal worms.

The odds of being infected were also higher among children with poor and average knowledge of STH. This underscores the importance of providing health education on STH in schools. Schools provide an opportune setting for delivering health information so that the most susceptible age groups are reached. Health education focusing on STH delivered in schools may help strengthen students’ knowledge and awareness about these parasites in general [42], including the perceived benefits of deworming [43].

The prevalence of any STH (A. lumbricoides and/or T. trichiura) was significantly higher in children attending urban compared to rural schools. This observation supports previous reports showing A. lumbricoides and T. trichiura are more prevalent in urban areas whereas hookworm is more common in rural areas [4447]. This higher prevalence is likely due to overcrowding, inadequate supply of clean water and poor sanitation. Thus, regular deworming and health education programmes targeting students and their parents across both rural and urban settings should be emphasized. Although, the common source of transmission for the three STH species is through contaminated soil, it can be noted that the mechanism through which the infective stages enter the human host varies. For A. lumbricoides and T. trichiura, the route of transmission is through feacal-oral, while infection with hookworm (N. americanus and A. duodenale) can be acquired through skin penetration of larvae from feacal contaminated soil. Risk factors for A. lumbricoides and T. trichiura include inadequate access to clean water supply and ingestion of contaminated food [48]. Hookworm was more associated with inadequate sanitation but, in the case of A. duodenale, infection can also be acquired orally through contaminated food and water [48].

Despite the majority of the study participants reported to have access to household toilets and improved source for drinking water, the prevalence of any STH infections was still high. As earlier stated, since the information on the functionality of toilets and level of sanitary condition at the household level were not collected in the present study, it may be possible that these unmeasured factors facilitate STH transmission. The low prevalence of hookworm infection observed in this study however, may suggests that there is a limited feacal contamination in the external environment leading to a decreased risk of infection for hookworm within the study area. We did not observe any association between STH infection and the following variables: sex, main source of drinking water, type of toilet used, and attitude and practices towards STH among schoolchildren, findings contrasting with previous reports [49,50]. Risk factors associated with STH infections could, however, vary from one location to another depending on the area’s topographical landscape, environmental sanitation, lifestyle and culture of the resident population.

The prevalence of stunting (20.2%) and being underweight (19%) was lower than reported in the 2018 National Nutrition Survey of the FNRI where 25% and 24.5% of the schoolchildren (aged 6–10 years) were underweight and stunted, respectively [17]. These estimates were also found to be lower in previous studies conducted locally [24,25,51] and in other countries [52,53]. The prevalence of wasting (9.5%) in this study, however, was slightly higher than the 2018 national estimate of 7.6% [17] but lower than reported elsewhere [24,5153]. Although, the prevalence estimates for stunting, being underweight and wasting reported in this study may be lower than previous estimates, they are still regarded as public health problems according to WHO criteria [54]. In addition, the prevalence of anaemia among study participants (13%) was classified as a mild public health problem based on WHO criteria and did not differ markedly from that reported in the 2018 national survey for children aged 9–10 years (12.4%) but was lower than reported in an earlier local study [28] and in other countries [52,53]. These discrepancies maybe due to differences in the dietary intake of the children, socio-economic factors, and/or other risk factors for malnutrition in schoolchildren [52]. The magnitude of malnutrition reported in this study indicates the need for interventions to avert the risk of malnutrition in schoolchildren.

It is notable that we found strong evidence of associations between any STH and stunting and underweight outcomes even with low prevalence of moderate to high intensity, after controlling for the effects of important confounders including age, sex, SES, rural/urban classification of schools, and the presence of anaemia and taking into account within school clustering. These outcomes demonstrate that schoolchildren infected with any STH were more likely to develop stunting and become underweight, results consistent with findings from other epidemiological studies involving schoolchildren in Malaysia [52], Peru [55] and China [56]. As shown previously, STH infection is associated with low food intake, impaired absorption of nutrients and altered metabolism resulting in poor growth and nutritional loss [7,57]. Although, there is not much evidence to support the malabsorption of nutrients as a mechanism contributing to underweight in STH-infected individuals, some reports have shown that A. lumbricoides lives in the gut where it can interferes with the nutritional absorption and cause damage to intestines resulting in symptoms such as diarrhoea, vomiting and consequently weight loss [7,5759].

We also found SES as significant independent predictor for both stunting and underweight. This is expected given the long synergy between poverty and malnutrition. Meanwhile, we observed that the risk of stunting and wasting increased with age. Anaemia additionally was identified as a significant independent predictor of being underweight. This maybe due to an independent relationship between anaemia and being underweight (as shown to be related to micronutrient deficiency including iron deficiency [60,61]). We observed no significant relationship between STH and wasting, an unsurprising finding given that wasting is a measure of current or acute malnutrition; studies in Timor Leste [62] and South Ethiopia [53] showed similar results. Furthermore, this absence of effect may have been due to the high prevalence of light intensity infections.

Furthermore, we found no significant relationship between STH infection and anaemia after controlling for age, sex, SES, and rural or urban classification of schools. This lack of effect may have been due to the low prevalence of high-intensity STH infections, the low prevalence of hookworm infection, or other unmeasured risk factors for anaemia inherent in the study population. Anaemia in children can be caused by other contributing factors such as deficiencies in micronutrients, including iron, vitamin A, Vitamin B12 or folate, malaria or schistosome infection, or genetic risk (e.g., sickle cell, α-thalassemia) [63]; although the study area is not endemic for malaria or schistosomiasis, exclusion of the other variables in the model may have influenced the results we report.

Another potential limitation of this study was the cross-sectional design we employed. As a result, we were unable to assess any causal relationship between STH and the observed risk factors, or between STH infection and the indices of malnutrition. The STH infection reported here may not necessarily be indicative of previous or chronic infection. In addition, while we have adjusted for potential confounders in the analysis, the risk for residual confounding may be possible based on the risk of exposure to STH infection and nutritional indices and/or anemia not included in the SES variable. Data on parents’ level of education and/or family composition (i.e., crowding index) that might have been important in constructing the SES variable were not collected in this study, a research gap that needs to be considered in future investigations. The use of the KK procedure for the diagnosis of STH is also a limitation. Although recent studies suggest that the method is reasonably accurate for A. lumbricoides and T. trichiura, it can result in low sensitivity to detect hookworm infection, particularly when faecal samples are not examined immediately [11,64,65]. Despite these limitations, the study has important strengths such as the robust statistical approach employed with adjustment for school clustering and the multiple covariates in the models.

The current WHO strategy for STH control in children is to continually treat pre-school-aged children (PSAC) and school-aged children (SAC) once or twice a year depending on prevalence [35]. Questions have been raised on the potential benefits of deworming based on nutritional indicators, the impact on haemoglobin levels, cognition, school performance and mortality following a recent Cochrane Database Systematic Review by Taylor-Robinson et al., which concludes that “there’s substantial evidence that deworming does not improve average height, haemoglobin, cognition, school performance, or mortality” [66]. However, the report’s conclusions have been disputed due to the methods and study selection criteria employed [6769] and/or concerns regarding whether systematic review methodology should be applied to STH studies due to the heterogeneity of STH prevalence of different species in different settings [69]. An article by Campbell et al. in 2016 [69] highlights the importance of appropriately designed studies that are powered to detect direct morbidity effects due to STH to strengthen evidence for deworming. Although the present study used cross-sectional data, the strength of associations between STH infection and child health outcomes (i.e., stunting and being underweight) observed in this study is striking and highlights the importance of continuous investigations on the impact of STH on child morbidity. Given that stunting and wasting are both indicator of long term (chronic) undernutrition (the latter’s an indicator for acute also), our cross-sectional data, may better reflect the accumulated morbidity of STH infection as opposed to RCTs or longitudinal studies with short period of follow-ups. To shed more light on this issue, future research should centre on the health effects of STH infections and of repeated doses of deworming provided over several years to assess the cumulative benefits of deworming.

The strong associations we report also suggest the need to address both STH infections and malnutrition in schoolchildren. There are existing programs currently available in the Philippines targeting STH infections (i.e., a nationwide school-based MDA program [16]) and malnutrition (school-based feeding program (SBFP) for severely wasted children [70]). Despite years of implementation, as consistently reported in a number of studies conducted across the country, the STH infection prevalence has continued to be high in schoolchildren [813] and nutritional improvements among children have not been sustained [70], indicating some challenges in the two programs. Although, it is difficult to draw firm conclusion about the impact of the MDA on STH infections levels from this study, the prevalence of moderate to heavy intensity infections observed in this study were lower compared to earlier studies, likely reflecting ongoing MDA. Thus, to ensure sustainable control of STH infections, other interventions are required. Our findings support the need for a holistic STH and nutrition programme in the Philippines. Uninterrupted deworming, complemented by provision of appropriate health education targeting parents and schoolchildren, improvements in sanitation facilities, and sanitation and hygiene practices, and a sustainable nutrition program, can provide the effective STH control measures required to improve the health and well-being of Filipino schoolchildren.

Supporting information

S1 Table. Attitude and practices of schoolchildren towards STH infection, in Laguna Province, the Philippines.

https://doi.org/10.1371/journal.pntd.0010008.s001

(DOCX)

Acknowledgments

The authors are grateful to the teachers, parents and students of the 40 schools in the province of Laguna who participated in the study. We also thank the officials of the DepEd and DOH in Laguna for their assistance in the conduct of the study. Thanks are also given to the Magic Glasses Philippines survey staff for their efforts in the data collection.

References

  1. 1. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37. pmid:24447578
  2. 2. WHO. Ending the neglect to attain the Sustainable Development Goals–A road map for neglected tropical diseases 2021–2030 Geneva: World Health Organization; 2020. Licence: CC BY-NC-SA 3.0 IGO.2020 [Available from: https://www.who.int/neglected_diseases/Ending-the-neglect-to-attain-the-SDGs—NTD-Roadmap.pdf?ua=1.
  3. 3. DALYs GBD, Collaborators H. Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388(10053):1603–58. pmid:27733283
  4. 4. Diseases GBD, Injuries C. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396(10258):1204–22. pmid:33069326
  5. 5. WHO. Soil- transmitted helminth infection 2018 [cited 2018 9 October 2018]. Available from: http://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections.
  6. 6. Brooker S. Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers—a review. Int J Parasitol. 2010;40(10):1137–44. pmid:20430032
  7. 7. Hall A, Hewitt G, Tuffrey V, de Silva N. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr. 2008;4 Suppl 1:118–236. pmid:18289159
  8. 8. Mationg MLS, Tallo VL, Williams GM, Gordon CA, Clements ACA, McManus DP, et al. The control of soil-transmitted helminthiases in the Philippines: the story continues. Infect Dis Poverty. 2021;10(1):85. pmid:34118990
  9. 9. Belizario VY Jr., Totanes FI, de Leon WU, Ciro RN, Lumampao YF. Sentinel surveillance of soil-transmitted helminthiasis in preschool-aged and school-aged children in selected local government units in the Philippines: follow-up assessment. Asia Pac J Public Health. 2015;27(2):NP1604–15. pmid:23572379
  10. 10. Belizario VYJ, Ng , Janice V., Amarillo , Maria Lourdes E., delos Trinos ,John Paul Caesar R., Reyes , Maureen R., Fudalan,Oscar High Burden of Soil-transmitted Helminths in preschool-age children in Masbate: a decade of implementation of the integrated helminth control program in the Philippines Southest Asian J Trop Med Public Health. 2016;47(4):667–79.
  11. 11. Mationg MLS, Gordon CA, Tallo VL, Olveda RM, Alday PP, Renosa MDC, et al. Status of soil-transmitted helminth infections in schoolchildren in Laguna Province, the Philippines: Determined by parasitological and molecular diagnostic techniques. PLoS Negl Trop Dis. 2017;11(11):e0006022. pmid:29108026
  12. 12. Ross AG, Olveda RM, McManus DP, Harn DA, Chy D, Li Y, et al. Risk factors for human helminthiases in rural Philippines. Int J Infect Dis. 2017;54:150–5. pmid:27717859
  13. 13. Ross AG, Papier K, Luceres-Catubig R, Chau TN, Inobaya MT, Ng SK. Poverty, Dietary Intake, Intestinal Parasites, and Nutritional Status among School-Age Children in the Rural Philippines. Trop Med Infect Dis. 2017;2(4).
  14. 14. Belizario VY Jr., Ng JV, Amarillo MLE, delos Trinos JPCR, Reyes MR, Fudalan O. High burden of soil-transmitted helminthiases in preschool-age children in masbate: A decade of implementation of the integrated helminth control program in the Philippines. Southeast Asian J Trop Med Public Health. 2016;47(4):667–79.
  15. 15. DOH. Administrative Order 2006–0028. Strategic and operational framework for establisng integrated Helminth Control Program 2006 [Available from: https://dmas.doh.gov.ph:8083/Rest/GetFile?id=336683.
  16. 16. Education Do. DM 28, s. 2007- Implementation of the mass deworming program in all public elementary schools nationwide. 2007 [Available from: http://www.deped.gov.ph/wp-content/uploads/2018/10/DM_s2007_028.pdf.
  17. 17. Vargas MB. Nutritional Status of Filipino Pre-school and School Children. Department of Science and Technology—Food and Nutrition Research Institute; 2018.
  18. 18. de Benoist B, McLean E, Egli E, Cogswell M. Worldwide prevalence of anaemia 1993–2005: WHO Global Database on Anaemia World Health Organization; 2008.
  19. 19. Ricci JA, Becker S. Risk factors for wasting and stunting among children in Metro Cebu, Philippines. Am J Clin Nutr. 1996;63(6):966–75. pmid:8644694
  20. 20. Salvacion A. Exploring Determinants of Child Malnutrition in Marinduque Island, Philippines. Hum Ecol. 2017;45:853–63.
  21. 21. Capanzana MV, Aguila DV, Gironella GMP, Montecillo KV. Nutritional status of children ages 0–5 and 5–10 years old in households headed by fisherfolks in the Philippines. Arch Public Health. 2018;76:24. pmid:29686867
  22. 22. Magnani RJ, Mock NB, Bertrand WE, Clay DC. Breast-feeding, water and sanitation, and childhood malnutrition in the Philippines. J Biosoc Sci. 1993;25(2):195–211. pmid:8478369
  23. 23. Adair LS, Guilkey DK. Age-specific determinants of stunting in Filipino children. J Nutr. 1997;127(2):314–20. pmid:9039833
  24. 24. Papier K, Williams GM, Luceres-Catubig R, Ahmed F, Olveda RM, McManus DP, et al. Childhood malnutrition and parasitic helminth interactions. Clin Infect Dis. 2014;59(2):234–43. pmid:24704723
  25. 25. Belizario VY Jr., Totanes FI, de Leon WU, Lumampao YF, Ciro RN. Soil-transmitted helminth and other intestinal parasitic infections among school children in indigenous people communities in Davao del Norte, Philippines. Acta Trop. 2011;120 Suppl 1:S12–8.
  26. 26. Belizario V Jr., Delos Trinos J, Sison O, Miranda E, Molina V, Cuayzon A, et al. High burden of soil-transmitted helminth infections, schistosomiasis, undernutrition, and poor sanitation in two Typhoon Haiyan-stricken provinces in Eastern Philippines. Pathog Glob Health. 2021:1–11.
  27. 27. Tengco LW, Rayco-Solon P, Solon JA, Sarol JN Jr., Solon FS. Determinants of anemia among preschool children in the Philippines. J Am Coll Nutr. 2008;27(2):229–43. pmid:18689554
  28. 28. Ng JV, Belizario VY Jr, Claveria FG. Determination of soil-transmitted helminth infection and its association with hemoglobin levels among Aeta schoolchildren of Katutubo Village in Planas, Porac, Pampanga. Phil Sci Lett. 2014;7:73–80.
  29. 29. Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, et al. The synergistic effect of concomitant schistosomiasis, hookworm, and trichuris infections on children’s anemia burden. PLoS Negl Trop Dis. 2008;2(6):e245. pmid:18523547
  30. 30. Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis JD, Mor V, et al. Functional significance of low-intensity polyparasite helminth infections in anemia. J Infect Dis. 2005;192(12):2160–70. pmid:16288383
  31. 31. Mationg MLS, Williams GM, Tallo VL, Olveda RM, Aung E, Alday P, et al. Determining the Impact of a School-Based Health Education Package for Prevention of Intestinal Worm Infections in the Philippines: Protocol for a Cluster Randomized Intervention Trial. JMIR Res Protoc. 2020;9(6):e18419. pmid:32584263
  32. 32. Mationg MLS, Williams GM, Tallo VL, Olveda RM, Aung E, Alday P, et al. “The Magic Glasses Philippines”: a cluster randomised controlled trial of a health education package for the prevention of intestinal worm infections in schoolchildren. The Lancet Regional Health—Western Pacific. 2021.
  33. 33. PSA. Highlights of the population density of the Philippines 2020 Census of Population and Housing (2020 CPH) 2021 [Available from: https://psa.gov.ph/content/highlights-population-density-philippines-2020-census-population-and-housing-2020-cph.
  34. 34. Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972;14(6):397–400. pmid:4675644
  35. 35. WHO. Helminth control in school-age children: a guide for managers of control programmes. Geneva: World Health Organization2011.
  36. 36. WHO. Growth reference data for 5–19 years [15 March 2020]. Available from: https://www.who.int/tools/growth-reference-data-for-5to19-years/application-tools.
  37. 37. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85(9):660–7. pmid:18026621
  38. 38. WHO. Haemoglobin concentration for diagnosis of anaemia and assessment of severity Geneva: World Health Organization; 2011.
  39. 39. Filmer D, Pritchett LH. Estimating wealth effects without expenditure data—or tears: an application to educational enrollments in states of India. Demography. 2001;38(1):115–32. pmid:11227840
  40. 40. WHO/UNICEF. Progress on household drinking water, sanitation and hygiene 2000–2020: Five years into the SDGs: Geneva: World Health Organization (WHO) and the United Nations Children’s Fund (UNICEF). Licence: CC BY-NC-SA 3.0 IGO.; 2021 [Available from: file://mhsdata.anu.edu.au/desktop$/u6617474/Desktop/jmp-2021-wash-households-LAUNCH-VERSION%20(1).pdf.
  41. 41. WHO. Soil-transmitted helminthiases: eliminating as public health problem soil-transmitted helminthiases in children: progress report 2001–2010 and strategic plan 2011–2020. World Health Organization; 2012.
  42. 42. Bieri FA, Gray DJ, Williams GM, Raso G, Li YS, Yuan L, et al. Health-education package to prevent worm infections in Chinese schoolchildren. N Engl J Med. 2013;368(17):1603–12. pmid:23614586
  43. 43. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M. Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis. 2013;7(9):e2397. pmid:24069469
  44. 44. Oninla SO, Owa JA, Onayade AA, Taiwo O. Intestinal helminthiases among rural and urban schoolchildren in south-western Nigeria. Ann Trop Med Parasitol. 2007;101(8):705–13. pmid:18028732
  45. 45. Pullan RL, Brooker SJ. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors. 2012;5:81. pmid:22537799
  46. 46. Phiri K, Whitty CJ, Graham SM, Ssembatya-Lule G. Urban/rural differences in prevalence and risk factors for intestinal helminth infection in southern Malawi. Ann Trop Med Parasitol. 2000;94(4):381–7. pmid:10945048
  47. 47. Kattula D, Sarkar R, Rao Ajjampur SS, Minz S, Levecke B, Muliyil J, et al. Prevalence & risk factors for soil transmitted helminth infection among school children in south India. Indian J Med Res. 2014;139(1):76–82. pmid:24604041
  48. 48. Echazu A, Bonanno D, Juarez M, Cajal SP, Heredia V, Caropresi S, et al. Effect of Poor Access to Water and Sanitation As Risk Factors for Soil-Transmitted Helminth Infection: Selectiveness by the Infective Route. PLoS Negl Trop Dis. 2015;9(9):e0004111. pmid:26421865
  49. 49. Tekalign E, Bajiro M, Ayana M, Tiruneh A, Belay T. Prevalence and Intensity of Soil-Transmitted Helminth Infection among Rural Community of Southwest Ethiopia: A Community-Based Study. Biomed Res Int. 2019;2019:3687873. pmid:31915688
  50. 50. Pasaribu AP, Alam A, Sembiring K, Pasaribu S, Setiabudi D. Prevalence and risk factors of soil-transmitted helminthiasis among school children living in an agricultural area of North Sumatera, Indonesia. BMC Public Health. 2019;19(1):1066. pmid:31391023
  51. 51. Belizario VY Jr., Liwanag HJ, Naig JR, Chua PL, Madamba MI, Dahildahil RO. Parasitological and nutritional status of school-age and preschool-age children in four villages in Southern Leyte, Philippines: Lessons for monitoring the outcome of Community-Led Total Sanitation. Acta Trop. 2015;141(Pt A):16–24. pmid:25255966
  52. 52. Ahmed A, Al-Mekhlafi HM, Al-Adhroey AH, Ithoi I, Abdulsalam AM, Surin J. The nutritional impacts of soil-transmitted helminths infections among Orang Asli schoolchildren in rural Malaysia. Parasit Vectors. 2012;5:119. pmid:22704549
  53. 53. Molla E, Mamo H. Soil-transmitted helminth infections, anemia and undernutrition among schoolchildren in Yirgacheffee, South Ethiopia. BMC Res Notes. 2018;11(1):585. pmid:30103797
  54. 54. WHO. Nutrition Landscape Information System (NLIS) country profile indicators: interpretation guide.; 2010 27 April 2021.
  55. 55. Casapia M, Joseph SA, Nunez C, Rahme E, Gyorkos TW. Parasite risk factors for stunting in grade 5 students in a community of extreme poverty in Peru. Int J Parasitol. 2006;36(7):741–7. pmid:16650426
  56. 56. Liu C, Luo R, Yi H, Zhang L, Li S, Bai Y, et al. Soil-Transmitted Helminths in Southwestern China: A Cross-Sectional Study of Links to Cognitive Ability, Nutrition, and School Performance among Children. PLoS Negl Trop Dis. 2015;9(6):e0003877. pmid:26110518
  57. 57. Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli AF, Savioli L. Controlling soil-transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Negl Trop Dis. 2008;2(3):e126. pmid:18365031
  58. 58. de Gier B, Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, van de Bor M, et al. Species-Specific Associations Between Soil-Transmitted Helminths and Micronutrients in Vietnamese Schoolchildren. Am J Trop Med Hyg. 2016;95(1):77–82. pmid:27246448
  59. 59. Crompton DW, Nesheim MC. Nutritional impact of intestinal helminthiasis during the human life cycle. Annu Rev Nutr. 2002;22:35–59. pmid:12055337
  60. 60. Sumarmi Sri, Puspitasari Nunik, Handajani R, Wirjatmadi B. Underweight as a risk factor for iron depletion and iron deficient erythropoiesis among young women in rural areas of East Java, Indonesia. Mal J Nutr. 2016;22(2):219–32.
  61. 61. Engidaye G, Melku M, Yalew A, Getaneh Z, Asrie F, Enawgaw B. Under nutrition, maternal anemia and household food insecurity are risk factors of anemia among preschool aged children in Menz Gera Midir district, Eastern Amhara, Ethiopia: a community based cross-sectional study. BMC Public Health. 2019;19(1):968. pmid:31324244
  62. 62. Campbell SJ, Nery SV, D’Este CA, Gray DJ, McCarthy JS, Traub RJ, et al. Investigations into the association between soil-transmitted helminth infections, haemoglobin and child development indices in Manufahi District, Timor-Leste. Parasit Vectors. 2017;10(1):192. pmid:28424091
  63. 63. Chaparro CM, Suchdev PS. Anemia epidemiology, pathophysiology, and etiology in low- and middle-income countries. Ann N Y Acad Sci. 2019;1450(1):15–31. pmid:31008520
  64. 64. Dacombe RJ, Crampin AC, Floyd S, Randall A, Ndhlovu R, Bickle Q, et al. Time delays between patient and laboratory selectively affect accuracy of helminth diagnosis. Trans R Soc Trop Med Hyg. 2007;101(2):140–5. pmid:16824566
  65. 65. Tarafder MR, Carabin H, Joseph L, Balolong E Jr., Olveda R, McGarvey ST. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a ’gold standard’. Int J Parasitol. 2010;40(4):399–404. pmid:19772859
  66. 66. Taylor-Robinson DC, Maayan N, Donegan S, Chaplin M, Garner P. Public health deworming programmes for soil-transmitted helminths in children living in endemic areas. Cochrane Database Syst Rev. 2019;9:CD000371. pmid:31508807
  67. 67. Montresor A, Addiss D, Albonico M, Ali SM, Ault SK, Gabrielli AF, et al. Methodological Bias Can Lead the Cochrane Collaboration to Irrelevance in Public Health Decision-Making. PLoS Negl Trop Dis. 2015;9(10):e0004165. pmid:26492178
  68. 68. de Silva N, Ahmed BN, Casapia M, de Silva HJ, Gyapong J, Malecela M, et al. Cochrane Reviews on Deworming and the Right to a Healthy, Worm-Free Life. PLoS Negl Trop Dis. 2015;9(10):e0004203. pmid:26492484
  69. 69. Campbell SJ, Nery SV, Doi SA, Gray DJ, Soares Magalhaes RJ, McCarthy JS, et al. Complexities and Perplexities: A Critical Appraisal of the Evidence for Soil-Transmitted Helminth Infection-Related Morbidity. PLoS Negl Trop Dis. 2016;10(5):e0004566. pmid:27196100
  70. 70. Tabunda A, Albert J.R., Angeles-Agdeppa I. Results of an impact evaluation study on DepED’s School-Based Feeding Program. PIDS Discussion Paper No. 2016–05. Philippine Institute for Development Studies; 2016.