Introduction

Widely distributed chronic infections caused by soil transmitted helminths (STHs) are one of the major public health concerns among people living in low and middle-income countries, particularly affecting the poorest and most deprived communities1. Almost 1.5 billion people are infected with STHs worldwide which includes infection of roundworm (Ascaris lumbricoides), whipworm (Trichuris trichiura), and hookworms (Necator americanus and Ancylostoma duodenale)2. World Health Organization (WHO) estimates that over 568 million school-going children and more than 267 million preschool children are at risk of STHs infections and are in urgent need of preventive interventions3.

Soil-transmitted helminth infections is a major public health concern among young children and studies have shown that STHs infections greatly impair their cognitive development and nutritional status4,5. The STHs usually do not present any symptoms unless there is a heavier infection which results into malnutrition, mal-absorption, abdominal pain, anemia, diarrhea, physical and mental growth retardation leading to important health consequences2,6,7. Severe STHs infections can cause even cognitive deficit and educational loss in school-aged children8,9. The risk of STHs infection is high in the regions with poor personal and environmental sanitation practices, eating and drinking of contaminated food and water, unhygienic toilet systems, handling or playing of infested soils and interaction with all these factors.

Importantly, the global burden of STHs infections is also linked with micronutrient such as vitamins, iron, and folate deficiencies and anemia which leads to reduced cognitive function and work capacity10. Malnutrition and anemia are associated with the severity of infections among the infected individuals, especially among pregnant women and school-age children. The synergistic existence of anemia, malnutrition and helminthiasis exert a negative impact on healthy growth of the infected individual11. Different types of STHs infection heavily affect nutritional status in different ways ranging from nutrient absorption to degree of mucosal damage12. Inadequate intake of Zn, Fe, and vitamin A predisposes individuals to helminth infections leading to nutritional deficiencies, thereby assisting helminth survival and severe infection13. Helminths feed on host tissues including blood which can cause loss of protein and iron of host. In addition, helminths may contest for vitamin A in the host intestine and some STHs cause loss of appetite whereas T. trichiura causes diarrhea and dysentery14. Low immune response due to malnutrition may increase susceptibility to STHs infections, therefore, nutritional supplementation is considered as a feasible means of controlling the morbidity due to STHs infections15.

The STHs infection is most prevalent among young children and women of reproductive age in the rural region of Nepal16,17,18 as a long standing health burden of the country19. In this light, a systemic review from Nepal found the pooled prevalence of 1.53% for hookworm, 4.23% for roundworm, and 2.89% for whip worm after 200420. The prevalence of STHs was reported to be much higher in rural areas (24.1%) compared to urban (18.7%), where the higher burden was influenced by various factors including poor sanitary habits, inadequate drinking water access, insufficient hand washing habit and walking barefoot in farming fields21,22,23. In addition, multiple micronutrients deficiency such as iron, vitamin A, iodine, folate, zinc and the condition of anemia has remained as a hidden hunger specifically, among young children of rural Nepal which has put them at a higher risk of severe STHs infections24,25. Pre-school-age children (PSAC) are also heavily infected by different helminths and acute complications are often reported such as Ascaris lumbricoides infection may lead to bowel obstruction, duodenal ulcer, hepatic abscesses and appendicitis26.

STHs, one of the neglected tropical disease (NTDs) is an important target of NTDs 2021–2030, a road map setup by the United Nations and the WHO to cover 90% of people in disease intervention programs by 203027. This highlights the importance of STHs control programs within the framework of universal health coverage to reduce the global burden promoting “leaving no one behind”. With this regard, Government of Nepal is working with multi stakeholders to tackle STHs infections through National Deworming Program, however diverse challenges exist due to unavailability of up-to-date national level epidemiological data to inform policy decisions and guide ongoing National Deworming and WASH (Water, Sanitation and Hygiene) programs in multiple provinces. To address this gap, our study aimed to assess the prevalence of STHs and its association with micronutrients deficiencies among children aged 6–59 months and non-pregnant women aged 15–49 years in Nepal, using nationally representative data.

Materials and methods

Study population and data sources

We used cross-sectional data from a nationally representative Nepal National Micronutrient Status Survey 2016 (NNMSS-2016). A detail methodology has been presented elsewhere28,29. The NNMSS-2016 study was conducted to provide up to date status on the basic health and nutrition status of 6–59 months old children and 20–49 years old non-pregnant women along with the associated demographic statistics. Stratified multistage cluster sampling without replacement approach was applied in the study in order to obtain the nationally representative estimates. Three geographical regions (Terai, Hill, and Mountain) and five development zones (Eastern, Central, Western, Mid-western, and Far western) were included hence the country was divided into 15 strata for this study (eastern mountain, eastern hills, eastern terai, central mountain, central hills, central terai, western mountain, western hills, western terai, mid-western mountain, mid-western hills, mid-western terai, far-western mountain, far-western hills and far-western terai). A minimum size of clusters was considered of 100 households and in case of wards having less than 100 households were merged with the adjacent wards whereas the clusters with more than 300 households were divided into the sub wards of 100 households. A total of 180 clusters (75 from the Terai and Hills each, and 30 clusters from the Mountains) were selected from the 15 strata considering the population proportion size30 where clusters (wards) were used as the primary sampling units (PSUs). A detail table of clusters is presented in the Table 1. A total of 24 households were selected from each cluster (24 × 180 = 4320) using a systematic random sampling. Cluster wise map was created by data collection team with the help of key informants such as teachers, female community health volunteers, etc. Subsequently, 24 households were selected systematically by the cluster supervisors prior the visit of field enumerators. A total of 4309 households were interviewed with the response rate of 99.7% (11 households were not available at the time of survey or refused to participate in this survey). Among the sampled households a total of 1728 children aged 6–59 months were eligible for interview and a total of 1709 children aged 6–59 months were interviewed with the response rate of 98.9% (1709/1728). Similarly, among 2160 non-pregnant women of aged 15–49 years were eligible for this study and 2144 were interviewed with the response rate 99.3% (2129/2144). Further, the participants with the missing values for STHs status among 6–59 months children (n = 174) and non-pregnant women (n = 117) were excluded from analysis. The final sample used in this analysis were 1535 children aged 6–59 months (89.8%) and 2012 non pregnant women (94.5%). Moreover, the non-response sample do not possess any systematic biases.

Table 1 Strata-wise distribution of sampling clusters.
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Data collection

The data collection was conducted in April–June 2016 using structure questionnaire. A total of 14 teams were deployed for this study. Each team was composed of a field supervisor, enumerators, and phlebotomist, and laboratory technicians altogether of 13 members to collect all the required data including the blood sample. Phlebotomists have collected blood (in EDTA and plain vials as per the standard protocol). Pathologists have collected urine and stool samples from the study participants. Non-fasted blood samples were collected since fasting was not possible in the survey. Pathologists have collected stool samples within 24 h of the interview. Further, the samples were shipped to the Kathmandu considering the standard protocol (maintaining the 2–8 °C cold chain), where they were stored at − 80 °C at the National Public Health Laboratory (NPHL) for further processing.

Anthropometry

Height/length-measuring board (Short-Board) was used to assess height/length and an electronic SECA digital scale (UNICEF Electronic Scale/Uniscale) was used to measure the weight of all recruited participants. The scale allows for the weighing of very young children through an automatic mother–child adjustment that eliminates the mother's weight while she is standing on the scale with her baby. After the measurement, the results of anthropometric measurements were immediately recorded on the respective questionnaire sheets31. In order to calculate anthropometric (z score) for children under five years the WHO Anthro survey analyzer version 1.0.3 was used. Body Mass Index (BMI) was calculated as body weight in kilogram divided by height in miters square (weight in kg/height in m2) of 20–49 years non-pregnant women.

Biological specimens

STHs infections among the enrolled children (aged 6–59 months) and non-pregnant women (aged 15–49 years) was assessed. The STHs infection caused by A lumbricoides, Trichuris trichura and hookworms was examined using the Kato-katz technique. Kato-Katz (KK) technique was adopted by the laboratory technicians to measure the type and intensity of STHs infections using fresh stool specimens. Fresh stool specimens were collected from participants next day morning of interview date. All the participants were instructed about the stool specimen collection procedure. Collected stool specimens were stored in the cold boxes, and later transferred to pathologists for testing of STHs. One gram of collected stool specimen was used to perform KK method in the study field and within 24 h of stool specimen collection, the pathologist prepared duplicate slide for microscopy of each specimen and counted helminths eggs using a portable microscope32. In addition, stool samples were used to detect the Helicobacter pylori antigen33.

Biomarkers of nutritional status

Photometric method using HEMOCUE Hb 301 analyzer was used to measure the hemoglobin (Hb). Hb < 11 g/dL were considered as the anemia for children aged 6–59 months whereas Hb < 12.0 g/dL were considered as anemia for non-pregnant women aged 15–49 years.

The sandwiched ELISA technique was used for the serum ferritin, Alpha-1 acid glycoprotein (AGP), C-reactive protein (CRP) and Retinol Binding Protein (RBP) at the VitMin Lab, Willstaett, Germany. Micronutrient parameters were adjusted according to the inflammation status. The antibodies used for this measurement were as follows: Capture antibodies: ferritin (Code A0133, Dako), RBP (Code A0040, Dako), and CRP (Code A0073, Dako Denmark). Detection antibodies: antiferritin-horseradish peroxidase (HRP) (Code P0145, Dako), anti-RBP-HRP (Code P0304, Dako), and anti-CRP-HRP (Code P0227, Dako). Iron deficiency was defined as if adjusted ferritin < 15.0 μg/L34.

Serum retinol was measured by HPLC is the WHO recommended indicator for vitamin A status. All the sample collected for this study were assessed to measure retinol-binding protein (RBP) using a sandwich ELISA at the VitMin Laboratory in Germany35. Vitamin A deficiency was defined as if RBP < 0.64 μmol/L35.

RBC folate was measured at Peking University, Institute of Reproductive and Child Health Laboratory (Beijing, China). Gold standard microbiological method for RBC folate concentration in RBC hemolysate was used following the protocol of O’Broin and Kelleher36. Risk of folate deficiency was classified as if RBC folate < 305.0 nmol/L based on risk of macrocytic anemia. We classified zinc deficiency as zinc < 66.0 μg/dL for nonfasted, morning samples (i.e. before 12 pm) and < 59.0 μg/dL for non-fasted, afternoon samples (i.e. after 12 pm) for non-pregnant 15–49 years women while we classified zinc deficiency as < 65.0 μg/dL for nonfasted, morning samples (i.e. before 12 pm) and < 57.0 μg/dL for non-fasted, afternoon samples (i.e. after 12 pm) for 6–59 months young children31.

Serum zinc concentration was determined by Microwave Plasma Atomic Emission Spectrometry (MP-AES) (Agilent Technologies; model 4200; series MY15260009/G8003A; Nitrogen generator: model 4107, series CN15270004; Autosampler: model SPS3, MY15250009/G8480A Series; Vapor generator accessory: VGA 77, series MY15260005/G8475A) at the Institute of Nutrition of Central American and Panama (INCAP) (Guatemala City, Guatemala)35.

Statistical analysis

All analyses were performed using Stata 15 (StataCorp LLC, Texas, USA)37. The reported values (percentage) were weighted by sample weights and 95% confidence intervals (CIs) were included for all the point prevalence considering the cluster sampling design. Logistic regression was used to assess unadjusted and adjusted odds ratio (AOR) and the 95% CIs of ORs. The bivariate association of STHs was assessed with the covariates: age, gender (children only), marital status (women only), lactation (women only), given birth in last five years (women only), level of education (women only), ecological zone (mountain, hills and terai), place of residence (rural and urban), and household wealth quintile (wealth quintile was calculated using household assets such as materials used for flooring, roofing, external walls, sources of drinking water, and possession of households amenities). Principal component analysis was used to calculate the wealth index and further ranked as the wealth quintile, caste/ethnicity (Brahmin or Chettri, Hill Dalit, Terai Dalit, Newar, Hill Janajati, Terai Janajati, Other Terai Castes, Muslims and Others), stunting (children only), wasting (children only), underweight (children only), BMI (women only), anemia (Hb < 12.0 g/dL), serum ferritin, risk of folate deficiency and zinc deficiency. Non-normally distributed variables were log transformed. Only significant association observed in bivariate logistic regression were included in the multivariate logistic regression model. Multicollinearity among the predictor variables were checked for variance inflation factors (VIFs). The predictors with the VIFs < 2.0 were only included in the multivariate logistic regression model. P < 0.05 was considered to be statistically significant.

Ethical approval and consent to participate

The ethical approval to conduct the survey was approved by the Ethical Review Board (ERB) of Nepal Health Research Council (NHRC) (Reg. No.: 201/2015), Ministry of Health and Population, Government of Nepal. Well informed written consent was obtained from all study participants before enrolled in the study. Parental consent was acquired for the participants of < 18 years to participate in the study at the time of survey in local community, eligible and interested adolescents parents’ written consent was ascertained individually. This study was conducted in accordance with the National Ethical Guidelines for Health Research in Nepal 2019 and the Declaration of Helsinki.

Results

Children aged 6–59 months

Overall, 12% (95% CI 10.2, 14.0) children aged 6–59 months had STHs (Table 2). The prevalence of A. lumbricoides was 10.7%, followed by hookworms and T. trichura were 1.4%, and 0.8%, respectively (Fig. 1).

Table 2 Socio-demographic and health characteristics of children aged 6–59 months by status of soil transmitted helminths, Nepal National Micronutrient Status Survey, Nepal, 2016.
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Figure 1
figure 1

Prevalence of soil transmitted helminths (STHs) among children aged 6–59 months and non-pregnant women aged 15–49 years, Nepal National Micronutrient Status Survey, 2016.

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Results of bivariate and multivariate analysis are presented on Table 3. In multivariate model, age ethnicity, anemia and zinc deficiency were associated with the occurrence of STHs. The likelihood of occurrence of STHs increases significantly with per month increase in age (AOR 1.02; 95% CI 1.00, 1.03). By ethnicity, compared to Brahmin/Chettri, the significantly higher odds of occurrence of STHs was observed among Terai Dalits (AOR 1.97; 95% CI 1.07, 3.63). Likewise, the significantly higher likelihood of occurrence of STHs was observed among the anemic 6–59-month children compared to non-anemic (AOR 1.74; 95% CI 1.12, 2.73). Similarly, those with zinc deficiency, the significantly higher odds of occurrence of STHs was observed compared to 6–59 months children who had normal zinc level (Fig. 2). All the non-significant predictors are presented in the Annex Table 1 (Supplementary Material).

Table 3 Predictors of soil transmitted helminths among children aged 6–59 months, Nepal National Micronutrient Status Survey, Nepal, 2016.
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Figure 2
figure 2

Graphical summary of the study design and major findings, figure was created with BioRender.com.

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Non pregnant women aged 15–49 years

Overall, 19% (95% CI 16.0, 21.4) non-pregnant women aged 15–49 years had STHs (Table 4). The prevalence of A. lumbricoids was 17.8%, whereas the hookworms and T. trichura were < 1% each (Fig. 1).

Table 4 Socio-demographic and health characteristics of non-pregnant women aged 15–49 years by status of soil transmitted helminths, Nepal National Micronutrient Status Survey, Nepal, 2016.
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In multivariate model, compared to unmarried, the significantly lower odds of STHs occurrence was observed among married/cohabitating women (AOR 0.60; 95% CI 0.39, 0.90). Compared to Brahmin/Chettri, the significantly lower odds of STHs occurrence was observed among Terai Janajatis women (AOR 0.45; 95% CI 0.23, 0.88) whereas the higher odds of occurrence was observed among Newars (AOR 1.65; 95% CI 1.07, 2.56). Similarly, the higher odds of occurrence of STHs was observed among non-pregnant women aged 15–49 years who had Vitamin A deficiency (AOR 4.72; 95% CI 1.00, 22.40) (Table 5). The wide range of 95% CI might be due to sample size as vitamin A was assessed only in sub sample; 653 of pre-school children and 529 of non-pregnant women. All the non-significant predictors are presented in the Annex Table 2 (Supplementary Material).

Table 5 Predictors of soil transmitted helminths among non-pregnant women aged 15–49 years, Nepal National Micronutrient Status Survey, Nepal, 2016.
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Discussion

More than one fourth of the global population is at risk of STHs infection, especially women of reproductive age (WRA), school aged children (SAC), and pre-school aged children (PSAC) are at higher risk38 and helminthic parasites are causing a considerable disease and disability in Nepal39,40. We evaluated the nationally representative samples (NNMSS-2016) collected from non-pregnant women (15–49 years) and children (6–59 months) covering all three ecological regions and determined the prevalence and associated potential risk factors of STHs infections in Nepal. Earlier cross-sectional studies were more focused on intestinal parasitic infections (IPIs) among young children of a particular area or school41,42 so, data on samples from all over Nepal including various age groups is very scanty. To the best of authors knowledge, this is the first study which includes nationwide data along with wider potential risk factors linked with STHs infections among young children and non-pregnant women.

Overall, 12% (95% CI 10.2, 14.0) of children aged 6–59 months had STHs infection where A. lumbricoides was the most common helminth (10.7%) followed by T. trichura (1.4%), and hookworms (0.8%), respectively. A study conducted among school children (9–12 years) of Bhaktapur, a neighboring district of Kathmandu has reported 27.7% prevalence of intestinal helminth parasites where A. lumbricoides (22.6%) was the most detected parasite followed by T. trichiura (6.06%)43,44 while prevalence was 42.5% among school going children in Kathmandu and A. lumbricoides (56.1%) and T. trichiura (17.5%) were the most common19. The low prevalence of STHs in our study could be due to nationwide deworming programs initiated in 2004 with vitamin A supplement focusing preschool children45. A findings from a meta-analyses by Kunwar et al. have observed a sharp decline in prevalence of STHs among school-aged children in Nepal in the last decade46. Higher rate (57.2%) of STHs infections was reported among school-aged children (6–12 years) from a village school of Indonesia47 where 62.39% of children used to play with dirt/soil each day. Similarly, high prevalence of STHs infections (75.6%) was reported from primary school going children of Utter Pradesh, India and A. lumbricoides (69.6%) was the most prevalent where open defecation, no use of soap for hand washing after defecation, and living in mud houses were the major predisposing risk factors associated with helminthic infections48. On the other hand, a cross-sectional national study conducted by Ediriweera et al. (2019) in Sri Lanka found only 0.97% of STHIs prevalence among primary school children (5–7 years) where 5946 children from 130 schools were included; while the country’s prevalence of STHIs was 6.9% among school children in 200349 and study highlights the importance of deworming program to reduce the burden of STHs infections in rural areas of Sri Lanka. In multivariate analysis of this study, age, ethnicity, anemia, and zinc deficiency were associated with the occurrence of STHs in children where probability of occurrence of STHs increases significantly with per month growth in age of the below five years children. Adding to this, the significantly higher odds of occurrence of STHs was observed among Terai Dalits compared to Brahmin/Chettri while in a cross-sectional study reported from Terai region of Nepal ethnicity was not significantly associated with the prevalence of geohelminth infection among individuals aged 20–60 years and the study showed prevalence of geohelminth closely associated with unhygienic behaviors and malnutrition50. Though there is no existing study focusing STHs among 6–59 months children, but it is plausible to mention that prevalence of geohelminth is high among this group belonging to poor socio-economic status in Nepal. Infection caused by STHs often coexist with micronutrient deficiencies among populations of low-income countries51. Status of micronutrient including zinc, hemoglobin, iodine, and vitamin A are associated with higher incidence of STHs infections, especially in children. Anemia and zinc deficiency showed significant association with the occurrence of STHs among children population of this study. Deficiency of certain micronutrients can make a person more susceptible to helminths infections, which can then affect the host's both nutritional and immune status. On the other hand, reduction of nutritional intake due to high intensity infections (many worms) can cause malaise and weakness leading to impaired physical development and fitness of growing age children52. Nearly 75% of nations with mild to severe Vitamin A deficiency (VAD) are co-endemic for STHs53 presenting two (VAD and STHs) overlapping global health issues so, coadministration of deworming drugs with supplement of vitamin A harness synergistic benefits to the people54,55. Pre-school children are at more risk of STHs and they need regular mass medication, termed as ‘preventive chemotherapy (PC)’56 and the WHO has recommended periodic large-scale PC when the prevalence of STHs infections surpasses a pre-defined threshold among school age children57. Approximately 49% of the WRA from the South East Asia were in need of preventive chemotherapy for STH in 201538. As per the data of WHO Preventive Chemotherapy and Transmission Control (PCT), Nepal has achieved the goal of PC in 2012/2013 with coverage of at least 75% of school aged children at risk. In this study, 82% of children have received deworming drugs. Positive association between A. lumbricoides infections and malnutrition among children aged 6–16 years was observed in a national survey conducted in Ecuador58. Similarly, zinc deficiency was significantly and negatively correlated with the Trichuris infection in Vietnamese school children aged 6–9 years where lower hemoglobin concentration was significantly correlated among children infected by Trichuris, hookworm, and multiple helminthic infections compared to uninfected ones59. Soil-transmitted helminths feed on host blood, and tissue in addition hookworms can cause intestinal blood loss which leads to anemia. Some of the STHs particularly T. trichiura also cause loss of appetite which reduce the nutrients intake and impairs the physical fitness of an individual60.

In multivariate analysis, compared to non-pregnant, the significantly lower odds of occurrence of STHs infections observed among married/cohabitating women (AOR 0.60; 95% CI 0.39, 0.90). Similarly, Newari ethnicity, and Vitamin A deficiency were predictors of STHs infections among non-pregnant women aged 15–49 years. Overall, 19% non-pregnant women aged 15–49 years had STHs where A. lumbricoids (17.8%) was the leading helminth, whereas hookworms and T. trichura was detected < 1%. A study conducted among adults (aged > 20, 256 men and 338 women) STHs infection was varied from 3.3% to 51.5% in Nepal where roundworm was the predominant cause of STHs infections. Surprisingly, nutritional status, occupation, and sociodemographic traits were not associated with the STHs infection but personal hygiene was the major risk factor among the enrolled population61. Anemia and hookworm infection are common problems among pregnant women so, WHO recommends deworming drugs for reproductive aged women and non-pregnant adolescent girls as a public health intervention in order to reduce the burden of STHs infection where prevalence of any STHs infection is ≥ 20% among reproductive aged women or adolescent girls48,62. In this study, STHs infection rate was more (49.9%) among women of Hilly zone compared to Terai (44.9%), and Mountain (5.2%). Similarly, women of rural area were more infected (85.1%) compared to women of urban area (8.4%) and only 34.2% of women have received deworming during the 6 months preceding the survey. In agreement with our study, prevalence of geohelminth infection was higher (76.2%) in rural districts of western Kenya among pregnant women and geohelminth infection was associated with use of polluted drinking water63. Similarly, higher prevalence (39%) of STHs infection was observed in a tribal area of southern India where people engaged in agriculture had higher odds (1.68, 95% CI 1.31–2.17, P < 0.001) of hookworm infection64. In contrast to current study, STHs infection was more in urban children aged 3–14 years than rural children and reported risk factors were having mothers of aged < 35 years, not wearing shoes, and sewage around residence65. A study reported from Nigeria, serum level of iron and vitamin A were significantly lower among STHs pregnant women and school-aged children66. Pregnant women may benefit from deworming drugs during their pregnancy, primarily by reducing anemia and a randomized, controlled trial study indicated deworming with mebendazole can be administered safely in antenatal care plan if hookworm infection is endemic67. In addition, STHs infection during pregnancy or early age of kids (< 1 year) is associated with poor cognitive outcomes of offspring68. Increasing evidence shows that prenatal exposure to STHs infection can impact the susceptibility of progeny, especially to allergy-associated disease69.

Strength and limitations

To the best of our knowledge, this study is the first nationwide epidemiological study to provide a comprehensive understanding of prevalence and determinants of STHs in Nepal. This study has some limitations. Echoing with previous cross-sectional studies, we could not establish causality between the covariates and incidence of STHs. We were unable to account for other potential confounders of STHs infections such as: personal hygiene, sanitation, environmental status, dietary habits, and thus residual confounding could not be excluded as predisposing factors associated with STHs infection in Nepal.

Conclusion

Despite nationwide deworming program and sanitation awareness, a noticeable prevalence of STHs among 6–59 months children and non-pregnant women was observed in Nepal, particularly children among Terai Dalits with anemic and zinc deficiency, and non-pregnant women among Newari ethnicity and non-pregnant women with Vitamin A deficiency. The findings of our analysis suggest high-risk populations should be on focus of deworming program, nutrition intervention, and mass administration of preventive chemotherapy along with supplement of vitamin A, iron tablets and Water, Sanitation and Hygiene (WASH) programs for non-pregnant women and young children. There is a need of holistic approach to achieve the progress towards eliminating STHs infection with efficient allocation of resources and developing disease tackling indicators in order to evaluate the dynamics of STHs transmission and infection in Nepal.