Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Search in posts
Search in pages
Filter by Categories
Brief Report
Case Report
Case Report and Review
Case Series
Commentary
Editorial
How do I do it
How I do it?
Invited Editorial
Letter to Editor
Letter to the Editor
Letters to Editor
Letters to the Editor
Mini Review
Original Article
Original Articles
Others
Review Article
Short communication
Short Paper
Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Search in posts
Search in pages
Filter by Categories
Brief Report
Case Report
Case Report and Review
Case Series
Commentary
Editorial
How do I do it
How I do it?
Invited Editorial
Letter to Editor
Letter to the Editor
Letters to Editor
Letters to the Editor
Mini Review
Original Article
Original Articles
Others
Review Article
Short communication
Short Paper
View/Download PDF

Translate this page into:

Review Article
15 (
1
); 4-19
doi:
10.1055/s-0042-1751319

Prevalence and Risk Factors of Soil-Transmitted Helminthic Infections in the Pediatric Population in India: A Systematic Review and Meta-Analysis

Department of Laboratory Medicine, All India Institute of Medical Sciences, New Delhi, India
Department of Pathology/Lab Medicine, All India Institute of Medical Sciences, Kalyani, West Bengal, India
Department of Pathology, Armed Forces Medical College, Pune, Maharashtra, India
Department of Biostatistics, All India Institute of Medical Sciences, New Delhi, India
Address for correspondence: Sudhanshu Shekhar, MD, Department of Pathology/Lab Medicine, All India Institute of Medical Sciences, Kalyani 741245, West Bengal, India (e-mail: sudsaiims@gmail.com).
Licence
This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon.
Disclaimer:
This article was originally published by Thieme Medical and Scientific Publishers Pvt. Ltd. and was migrated to Scientific Scholar after the change of Publisher.

Abstract

Soil-transmitted helminths (STH) is a major healthcare challenge in the pediatric age group affecting poor and deprived parts of our community. The main species that infect people are roundworm (AL, Ascaris lumbricoides), whipworm (TT, Trichuris trichiura), and hookworms (HW, Ancylostoma duodenale and Necator americanus). We aimed to estimate the pooled prevalence of STH infections in India in the pediatric age group (< 18 years) and assess the risk factors associated with STH in this age group. Three databases were searched (PubMed, Scopus, and Embase) up to February 16, 2021 with deliberate and inclusive search terms for original research articles estimating the prevalence of either of the three STH in India. Data extracted included individual prevalence of the three STH, prevalence of double or triple infections, and associated risk factors.

We identified systematically 1,408 publications, of which 44 were included for the final analysis, including studies from 20 states covering 34,590 children. In our study, the prevalence of AL ranged from 0.8 to 91% with a pooled prevalence of 25%, prevalence of TT ranged from 0.3 to 72% with a pooled prevalence of 13%, and for HW prevalence ranged from 0.2 to 80% with pooled prevalence of 10%. Two most important risk factors with higher odds ratio were open defecation practices or open latrine (odds ratio: 5.2) and washing hands without soap using water only (odds ratio: 2.49). Knowledge of areas with high prevalence of STH and associated risk factors would help in designing effective control strategies in the high-risk groups to prevent infection and aid in a drastic reduction of morbidity in children.

Keywords

Ascaris
hookworm
prevalence
soil-transmitted helminth
Trichuris

Introduction

Soil-transmitted helminths (STH) contribute significantly to intestinal helminthic infections and is a major healthcare challenge in pediatric age group. The main species that infect people are the roundworm (AL, Ascaris lumbricoides), the whipworm (TT, Trichuris trichiura), and hookworm (HW, Ancylostoma duodenale and Necator americanus). They constitute those nematodes/roundworms that are transmitted through soil contaminated with fecal matter. Adult worms live in the intestine and produce thousands of eggs every day. STH infections are transmitted by eggs and larvae present in human feces that contaminate soil in areas with poor sanitation. Roundworm and whipworm eggs are infective, whereas HW egg has to develop in larval form to be infective to humans. The eggs are ingested while consuming fruits and vegetables that are not properly washed or cooked or from contaminated water sources or due to poor hygiene of children who come more often in contact with soil and put hands in their mouth. The eggs of HW hatch in the soil and release larvae that mature into a form that actively penetrates the skin to cause infection. Therefore, people who have habit of walking barefoot on contaminated soil are more prone to HW infection. The preschool-aged children, school-aged children, and women of childbearing age are mainly at high risk of STH infections. Since these worms do not multiply in the human host, reinfection may occur only as a result of contact with infective stages in the environment. STH can be diagnosed by examination of stool sample using microscope for the presence of eggs. The risk of STH infection cannot be linked with any one factor because of coexistence and combined effect of multiple factors including environmental, behavioral, social, and biological, both at individual and community level.

STH infections are a major public health problem in tropical and subtropical countries affecting the poor and deprived parts of the community. Around 1.5 billion people globally are infected with STH infections. Worldwide 819 million people approximately are infected with Ascaris, 464 million with Trichuris, and 438 million with HW. More than 267 million preschool children and over 568 million school going children live in areas with increased transmission of these infections and thus are in need of preventive measures as well as treatment.[1] Asia contributes to almost 70% of the global prevalence of STH and within Asia the highest prevalence is seen in India (21%) followed by China (18%).[2,3] Infection is generally most prevalent among rural communities in warm and humid equatorial regions and where sanitation facilities are inadequate. However, infection can also occur in urban areas. Disability-adjusted life years caused by STHs are 5.2 million, and the majority 3.23 million (62%) are attributable to HW.[4]

To control the STH infections, it is important to target the high-risk population as well as areas where the prevalence is high. It can be achieved by periodic treatment that can reduce the intensity of infection of at-risk population living in these endemic areas. The World Health Organization (WHO) recommends periodic treatment with antihelmintics, without any previous diagnosis to all the at-risk people living in endemic areas. In 2018, more than 676 million school-aged children were given antihelminthics medicines in endemic countries that correspond to 53% of all children at risk.[1] Along with deworming, STH infections can be prevented by educating the community on healthy and hygienic practices and provision of access to basic sanitation facilities, though that may sometimes be difficult specially in resource poor settings.

With an objective of deworming all preschool and school-aged children between 1 and 19 years of age through schools and Anganwadi centers, the Ministry of Health and Family Welfare, Government of India launched the National Deworming Day on February 10 each year. The first round of this was conducted in February 2015.

Although previous studies or reviews are available on prevalence of STH in India, none of them conducted a meta-analysis and that too in children, the group that is at higher risk. Due to the high morbidity caused by STH infections, we intended to review, assess, and synthesize the literature on prevalence and risk factors of the three STH infections among children (< 18 years) in India. To the best of our knowledge, this is the first systematic review and meta-analysis addressing both the prevalence and risk factors of STH infections in the Indian context in this age group. This study will help in identifying the areas most affected with STH infections and identification of the most important risk factors to develop targeted prevention strategies.

Objective

We aimed to conduct a systematic review and meta-analysis to estimate the pooled prevalence of STH infections in India in pediatric age group (< 18 years). Our secondary objective was to assess the risk factors associated with STH in this age group.

Methods

This review was conducted in accordance with “Preferred Reporting Items for Systematic reviews and Meta-analysis–Protocols” (PRISMA-P)[5] and the “Meta-analysis of Observational Studies in Epidemiology' (MOOSE)” guidelines.[6] This study was registered with the International prospective register of systematic reviews “PROSPERO” [Registration no. CRD42021234126].

Eligibility Criteria

Criteria were established for eligibility of articles in the review before beginning the search.

Inclusion Criteria

All community-based observational studies reporting the prevalence of at least one STH among children (0—18 years) in India were included. Ascaris (AL), Trichuris (TT), and HW (Ancylostoma mostly found in India) were the three STH for which prevalence was noted.

Exclusion Criteria

Case reports, clinical/intervention studies, hospital-based studies, and review articles were excluded. Only community-based studies were included where the subjects were not having any previous diagnosis. Moreover, articles that were not fully accessible were excluded because of the inability to assess the quality of articles in the absence of full text.

Search Strategy and Data Extraction

Three databases were searched (PubMed, Scopus, and Embase) up to February 16, 2021 to do the literature search with the following search terms: (prevalence or incidence or epidemiology or risk factor or causal factor) and (helminth or STH or Ascaris or Trichuris or HW) and (India or Indian) and (pediatric or child or kid or baby). The reference lists of relevant articles obtained were screened for its suitability to be recruited into this review. No filters were used. Duplicates were removed. Two authors (PC and SS) independently conducted the search and screened the study title and abstract. The studies selected after screening the title and abstract were then screened further by full text selection. For articles related to the prevalence of STH—any one or all three, AL or TT or HW in the title and/or abstract, the full text was assessed further. Full-text selection was done with approval of both the authors. Disagreements during full-text selection were resolved by discussion and reaching consensus in the presence of third author (VKD).

The two authors (PC and SS) extracted the data and performed quality assessment of included studies using Microsoft Excel. One of the reviewers recorded the data from the selected studies into the extraction form using Excel, while the second reviewer verified the accuracy and completeness of the extracted data. Data was extracted under the headings: first author, year of publication, place, author of the study, age of study subjects, setting, month and year in which it was conducted, duration of the study, type of study, individual prevalence of the three STH, prevalence of double or triple infections, and the stool processing method used. The associated risk factors with the number of cases infected and not infected with STH both in exposed and nonexposed groups were noted. In studies where all age groups were included, data for pediatric age group was extracted and rest were excluded. For studies with multiple intestinal parasites, data for the STH (any available or all three) was extracted.

Quality Assessment:

The studies were assessed for the methodological quality based on the tool developed by Wong et al also used in a few other studies.[7,8] The checklist quality assessment tool for systematic reviews of observational studies (QATSO) (Supplementary Table S1) was used to assess the quality of searched articles by two independent investigators (PC and SS). The tool consists of 6 items that assess components in observation studies and whenever the information provided was not enough to assist in making judgement for a certain item, we agreed to grade that item with a “0” meaning high risk of bias. Each article's quality was graded as “good” if the score was 5 or 6 out of 6; or graded as “satisfactory” if the score was 3 or 4 out of 6, and “poor” if the score was 0, 1, or 2 out of 6. The studies were not excluded on basis of their quality.

Ethical approval was not required in this review as the work consisted of secondary data collection and analysis.

Data Analysis:

The analysis was done by STATA/se Version 13.0 statistical software. We presented results with tables and forest plots. The pooled prevalence of each STH was estimated with a random effect model by generating the pooled 95% confidence interval (CI) using the Der Simonian and Laird's methods. Heterogeneity among studies was assessed by calculating p-values for Higgins I2- statistics. I2 index (low is < 25%, moderate 25–50%, and high > 50%) indicated the percent of total discrepancy due to variation between the studies. The risk factors for STH infection were reported in odds ratio (OR) with 95% CI by using a random effect model. Begg's funnel plot was used for evaluating the possibility of publication bias (Supplementary Fig. S1).

Results:

Literature Searches and Selection

We identified systematically 1,408 publications, of which 44 were included for the final analyses. The details of our search strategy are depicted in Supplementary Table S2 and the flow of selection of studies for the review is shown in Fig. 1. Our initial search of electronic databases such as PubMed, Scopus, and Embase yielded 1,388 articles and 20 articles from other sources including extensive search of references of studies. Out of 1,408 articles, 436 were found to be in duplicate and were removed. Further on the basis of title and abstract, 861 articles were excluded. These were not found suitable according to our inclusion criteria. From the remaining studies that were selected, 48 full-text articles could not be obtained and had to be excluded. Sixty-three studies were initially selected. Full text for each of these 63 studies was read carefully. Nineteen articles were further excluded due to various reasons. Two were hospital-based/intervention studies, five had no separate data for pediatric population, three were lacking data for STH, and nine had to be excluded due to different reasons like data discrepancy in text and tables of articles. Finally, 44 articles published between 1968 and 2020 fulfilling the inclusion criteria were included. These studies reported the prevalence of at least one STH among pediatric age group in India.

Flowchart of selection of studies for the review. STH, soil transmitted helminths.
Fig. 1
Flowchart of selection of studies for the review. STH, soil transmitted helminths.

The characteristics of selected studies included in systematic review and meta-analysis are shown in Table 1. The sample size of the included studies ranged from 529 to 6,42110 with a total number of 34,590 participants for which stool samples were examined for the presence of one or more intestinal parasites. Data specifically matching our inclusion and exclusion criteria was extracted. Total of 18 studies had the data of prevalence for all three STH, 21 studies had data for at least two parasites, 2 studies had data only for AL, 1 only for TT, and 2 only for HW. For stool examination, the researchers in the given studies used direct microscopy by wet mount (saline and iodine), Kato-Katz technique and microscopy after stool concentration with methods like salt flotation, formol ether concentration, mini-FLOTAC, and zinc sulphate for parasite detection. Maximum number of studies, 18 (42% of the studies) were from North India, of which 8 were from Jammu and Kashmir, 3 from Delhi, 4 from Uttar Pradesh, 2 from Uttarakhand, and 1 from Haryana. From Northeast 3 (6.8%) studies were included, 2 from Sikkim, and 1 from Assam. In the central India only, two (4.5%) studies were included, one each from Chhattisgarh and Madhya Pradesh. Five (12.5%) studies were from Eastern India, three from West Bengal and one from Bihar and Orissa each. One of the studies was partly carried out in Uttar Pradesh and partly in Jharkhand. From the west part of India, 4 (9.1%) studies were included, two from Gujarat and one from Maharashtra and Rajasthan each. From the southern part of India, 11 (25%) studies were included, five from Tamil Nadu, three from Andhra Pradesh, two from Karnataka, and one from Puducherry. Children from all age groups 0 to less than 18 years were included in the studies.

Table 1 Characteristics of selected studies included in the systematic review and meta-analysis (N = 44)
Sl no. Author/year Study design Study duration Setting Location Sample size Age group (y) STH% Technique
AL TT HW Double inf Triple inf
1 Narain et al/2000[25] Cross sectional 1996–1998 Village Dibrugarh, Assam 168 0–10 26.8 Formalin—ether concentration
2 Subba and Singh/2020[12] Cross sectional Jan 2016–Dec 2016 School children East Sikkim 300 5–18 3 0.3 Nil Saline and Iodine mount, formalin ether concentration
3 Devi/2009[15] Cross sectional Feb 2008–Sep 2008 School children Dibrugarh, Assam 1029 5–13 63 19 1.7 Direct smear and formalin ether concentration
4 Wani and Ahmad/2009[26] Cross sectional April 2007–Oct 2007 School children Pulwama, Jammu & Kashmir 199 5–14 69.8 31.6 Nil Direct smear and zinc sulphate floatation concentration
5 Wani and Amin/2016[27] Cross sectional May 2013–Nov 2013 School children Shopian, Jammu & Kashmir 352 4–15 71.8 26.4 Nil Direct smear and zinc sulphate floatation concentration
6 Wani et al/2008 (a)[28] Cross sectional May 2006–Nov 2006 School children Anantnag, Baramulla, Budgam, Kupwara, Pulwama, and Srinagar, Jammu & Kashmir 382 5–15 63 54 Nil 39.26 Direct smear and zinc sulphate floatation concentration
7 Lone et al/2011[29] Cross sectional May 2009–Nov 2009 School children Budgam, Jammu & Kashmir 396 3–14 54.9 32.5 Nil Formalin ether concentration, Kato-Katz smear
8 Wani et al/2007 (a)[30] Cross sectional April 2006–Oct 2006 School children Srinagar Jammu & Kashmir 514 5–14 28.4 4.9 Nil Direct smear and zinc sulphate floatation concentration & stall egg counting technique
9 Wani et al/2008 (b)[31] Cross sectional March 2007–Nov 2007 Children from rural and urban areas Anantnag, Baramulla, Budgam, Kupwara, Pulwama, and Srinagar, Jammu & Kashmir 2256 0–15 68.3 27.9 NIL 1.8 Direct smear and zinc sulphate floatation concentration
10 Wani et al /2010[32] Cross sectional July 2008 – October 2008 School children Gurez valley, Bandipora, Jammu & Kashmir 352 1–15 71.8 26.4 Nil Simple smear and Kato-Katz thick smear
11 Wani et al/2007(b)[33] Cross sectional Kupwara, Jammu & Kashmir 312 4–15 69.23 30.76 Nil 22.1 Direct smear and zinc sulphate floatation concentration
12 Das et al/2019[9] Cross sectional Aug 2016–Sep 2016 Children from ICDS center Darjeeling, West Bengal 52 0.5–6 7.7 1.9 Nil Direct smear and zinc sulfate floatation and formalin-ether concentration
13 Chowdhury et al/1968[14] Cross sectional 1961–1963 Rural area Kolkata, West Bengal 261 0–15 80 Direct smear and salt flotation
14 Nawalinski et al/1978[34] Cross sectional March 1969–Dec 1970 Rural area Kolkata, West Bengal 4078 1–11 14 1.8 68.3 Martin-Beaver modification of the Kato-Katz thick-smear
15 Greenland et al/2015[16] Cross sectional Jan2011–Feb 2011 School children Araria, Aurangabad, Muzaffarpur and Gopalganj, Bihar 1157 4–17 52 5 42 26.7 1.8 Modified Kato-Katz
16 Mahapatra et al/2020[17] Cross sectional May 2015–Oct 2015 Slum children Bhubaneswar, Odisha 360 3–15 5.8 Nil 10.5 3.05 Direct smear and Kato-Katz
17 Bora et al/2006[35] Cross sectional Aug 2005 Hilly area children Pauri Garhwal, Uttarakhand 257 9–10 28.8 1.9 5.1 4.3 Modified Kato-Katz
18 Bansal et al/2018[18] Cross sectional School children Rishikesh, Uttarakhand 461 <10 0.8 Nil 2.1 Concentration by saturated salt Solution and saline & iodine mount
19 Awasthi et al/1997[36] Cross sectional Jan1995–July 1995 Children from anganwadi centers Lucknow, Uttar Pradesh 1040 1.5-3.5 11.9 Direct smear examination
20 Ganguly et al/2017[10] Cross sectional May 2015–August 2015 School children Uttar Pradesh 6421 <15 69.6 4.6 22.6 8.1 0.07 Double Kato-Katz
21 Bisht et al /2011[37] Cross sectional June 2008–Dec 2009 Community children Ghaziabad, Uttar Pradesh 335 1–14 2.3 1.8 1.2 Saline and Lugol iodine wet mount and formalin ether concentration
22 Awasthi et al/2008[23] Cross sectional Rural area Sant Ravidas Nagar, Uttar Pradesh and Khunti, Jharkhand 909 0.5–2 32.1 2.6 3.9 Formalin—ether concentration.
23 Yunus et al/1979[24] Cross sectional 1977 School children Aligarh, Uttar Pradesh 59 5–15 8.5 Nil 11.9 Direct smear examination
24 Chandi et al /2018[38] Cross sectional School children Durg, Chhattisgarh 250 6–15 19.2 Nil 10.3 Saline and iodine wet mount, formalin ether concentration
25 Ranjan et al/2015[39] Cross sectional Nov 2012–Jan 2013 School children Delhi 347 5–15 8.1 3.7 3.7 Kato-Katz technique
26 DattaBanik et al/1978[40] Cross sectional 1977 Preschool children of slum area Delhi 2493 0–5 8.4 1.4 2.7 Direct smear
27 Gupta et al /2020[19] Cross sectional Jan 2016–Dec 2016 Community children Delhi 250 6–14 54.4 4.8 Nil 4.4 Kato-Katz technique
28 Dhaka et al/2020[41] Cross sectional school children Rohtak, Haryana 300 6–10 14 Nil 5 Direct smear
29 Tripathi et al/2014[42] Cross sectional July 2013–August 2013 School children Bhopal, Madhya Pradesh 300 6–12 9.84 4.92 Direct smear examination
30 Choubisa et al/2012[43] Cross sectional Oct 2011–Sept 2011 Bhil tribe Udaipur, Rajasthan 120 0–15 5.8 Nil 1.6 Formalin ether concentration
31 Shobha et al/2013[20] Cross sectional Feb 2008–Dec 2008 Urban slum dweller Gujarat 518 1–14 2.5 Nil Nil Formalin ether concentration
32 Lakhani et al /2012[44] Cross sectional June2013–Oct 2013 School children Vadodra, Gujarat 140 6–12 3.6 0.7 2.1 Formalin ether concentration
33 Naish et al/2004[11] Cross sectional Dec 1997–Dec 1998 School children Vishakhapatnam, Andhra Pradesh 204 5–9 91 72 54 Modified formalin ether sedimentation
34 Paul et al/1999[45] Cross sectional 1993–1994 School children Vishakhapatnam, Andhra Pradesh 217 7–13 73 66 9 50.7 8 Formalin ethyl acetate sedimentation
35 Rangaiahagari et al/2013[46] Cross sectional June 2006–August 2006 School children Amalapuram, Andhra Pradesh 208 5–13 2.9 1.4 5.2 0.96 Formalin ether concentration
36 Aher and Kulkarni /2011[47] Cross sectional School children Ahemednagar, Maharashtra 624 6–12 1.9 0.9 Saline and Lugol iodine wet mount
37 Anbumani et al/2011[48] Cross sectional Jan 2008 School children Kancheepuram, Tamil Nadu 358 5–10 38.8 13.9 Nil 10 Direct microscopy and saturated sodium chloride floatation
38 Elkins /1984[49] Cross sectional Different social community Chennai, Tamil Nadu 491 1–12 60.3 62.3 30.5 Merthiolate iodine formaldehyde Conc Tech, Quant Stoll egg counting technique
39 Kattula et al/2014[50] Case–control December 2008–August 2009 School children Vellore, Tamil Nadu 3706 6–14 1.2 0.8 6.3 Saline and iodine wet preparation, match master egg counting screening
40 Gopalakrishnan et al/2018[51] Cross sectional January 2017–March 2017 School children Kancheepuram, Tamil Nadu 250 13–18 3.2 Nil 4.4 Direct microscopic examination
41 Christu Rajan et al /2020[13] Cross-sectional Nov 2015–July 2015 School children Coimbatore, Tamil Nadu 610 5–14 6.9 0.7 0.2 Saline wet mount and iodine wet mount, formalin ether sedimentation
42 Ragunathan et al/2010[21] Cross-sectional March2006–Sept 2006 School children Puducherry 1172 5–10 17.5 5.4 12.5 1.8 0.3 Saline and iodine wet preparation, formalin ether sedimentation, Hirada Mori
43 Golia /2014[52] Cross-sectional June 2003–Sept 2013 School children Bangalore, Karnataka 258 6–12 8.1 5.4 1.2 saline and iodine wet mounts, formalin ether sedimentation
44 Panda et al/2012[22] Cross-sectional Dec 2008–Jan 2009 School children Bangalore, Karnataka 124 6–9 4.8 Saline and iodine wet mount

Abbreviations: AL, Ascaris lumbricoides; HW, hookworm; TT, Trichuris trichiura; STH, soil-transmitted helminths.

Quality Assessment

According to our quality assessment criteria, 32 publications out of 44 had score 3 or 4 indicating they were of moderate quality, 10 had a score of 5 or 6 indicating high quality, and the remaining 2 were of low quality with a score of zero or one or two. The results of quality assessment of studies are shown in Supplementary Table S3.

Population Characteristics

A total of 34,590 children from different studies were included in this analysis. Twenty-nine out of 44 studies (66% of total studies) were done on school children. The pooled prevalence of AL was estimated to be (n = 41 studies) 25% (95% CI: 16-35%) with substantial heterogeneity (I2 = 99.7%, p < 0.05); for TT (n = 31 studies) 13% (95% CI: 8–18%) with substantial heterogeneity (I2 = 99.4%, p < 0.05); and for HW (n = 29 studies) 10% (95% CI: 4–18%) with substantial heterogeneity (I2 = 99.6%, p < 0.05). Prevalence of double infections (n = 12 studies) was 11% (95% CI: 7–25%) with substantial heterogeneity (I2 = 99.09%, p < 0.05), triple infection (n = 4 studies) 1% (95% CI: 0–4%) with substantial heterogeneity (I2 = 97.0%, p < 0.05). Forest plots of pooled prevalence are given in Fig. 2. Prevalence of AL ranged from 0.8 to 91%.[11] For TT, the prevalence ranged from 0.3[12] to 72%.[11] For HW, the prevalence ranged from 0.2[13] to 80%.[14] Regional distribution of the three STH has been plotted in Figs. 35.

Forest plots showing pooled prevalence of (A) Ascaris, (B) Trichuris, (C) hookworm, (D) double soil transmitted helminthic infection, (E) triple soil transmitted helminthic infection. CI, confidence interval; ES, economic status.
Fig. 2
Forest plots showing pooled prevalence of (A) Ascaris, (B) Trichuris, (C) hookworm, (D) double soil transmitted helminthic infection, (E) triple soil transmitted helminthic infection. CI, confidence interval; ES, economic status.
Map of India showing percentage prevalence of Ascaris.
Fig. 3
Map of India showing percentage prevalence of Ascaris.
Map of India showing percentage prevalence of Trichuris.
Fig. 4
Map of India showing percentage prevalence of Trichuris.
Map of India showing percentage prevalence of hookworm.
Fig. 5
Map of India showing percentage prevalence of hookworm.

Pooled prevalence from studies in different parts of India is as shown in Supplementary Table S4. Maximum prevalence of AL was seen in Northeast and northern parts of India that are 46 and 35%, respectively. TT was found to be maximum in southern India and constituted 19% of the study population. Highest prevalence of HW was seen in eastern part of India (49%).

Risk Factors Analysis

Risk factors associated with STH were analyzed in this meta-analysis. Though previous studies reported association of multiple risk factors with STH and other intestinal parasitic infections, data specific to our inclusion criteria is shown here. The more commonly studied risk factors included gender (10 articles),[10,13,15-22] place of defecation whether in open or sanitary latrines (7 articles),[10,13,15-17,23,24] hand washing after defecation with water only or soap and water (6 articles),[10,13,15-17,23] socioeconomic status (SES) upper and middle versus lower (4 articles),[10,13,19,24] mother's education (4 articles),[10,13,16,19] barefoot walking (4 articles),[13,17,19,24] recent deworming(4 articles),[10,13,17,19] hygiene of finger nails (3 articles),[13,19,24] flooring earthen or cemented(3 articles),[10,13,15] religion (3 articles),[14,16,19] and hand washing before eating (3 articles).[13,16,19] OR was calculated and has been given in Table 2. For the factors including use of open defecation practices as compared to sanitary latrine, hand washing with water only versus with soap and water after defecation and having an earthen flooring in comparison to cemented flooring had OR more than 2 for getting STH infections. Forest plots for the risk factors associated with STH are as shown in Fig. 6. Males and females did not have higher odds over each other for getting STH infections. For the less commonly studied factors (in < 3 studies), OR of more than 2 was obtained in children with presence of anemia,[24] pica[19] in comparison to its absence, living in rural area on comparison with staying in urban area,[15] not attending school.[19] Absence of running water in latrine[15] and using a community bin rather than door to door disposal of waste[19] had higher odds of getting STH. Other factors like joint versus nuclear family,[13,19] father's education,[17,19] consumption of unwashed fruits and vegetables,[13] and using tap water over hand pump[15,23] did not have any association with STH infection and had OR around 1 or less than 1. Having a poor hygiene[13,19] in terms of not washing fruits and vegetables before eating and eating something that falls on floor and overcrowding[19] had higher odds of STH, 1.87 (95% CI: 0.31–11.37) and 1.83 (95% CI: 1.02–3.26), respectively.

Forest plots of risk factor analysis for soil transmitted helminthic infection showing odds ratio of (A) Males versus females. (B) Open latrine versus sanitary latrine. (C) Hand washing after defecation with water only versus with soap and water. (D) Socioeconomic status lower versus upper and middle. (E) Mother education below primary/ illiterate versus above primary. (F) Walking barefoot versus walking with footwear. (G) Recent deworming negative to recent deworming done. (H) Nails untrimmed versus trimmed. (I) Flooring earthen versus cemented. (J) Religion: Hindu versus other religions. (K) Poor hand wash habits versus good hand wash. CI, confidence interval; OR, odds ratio.
Fig. 6
Forest plots of risk factor analysis for soil transmitted helminthic infection showing odds ratio of (A) Males versus females. (B) Open latrine versus sanitary latrine. (C) Hand washing after defecation with water only versus with soap and water. (D) Socioeconomic status lower versus upper and middle. (E) Mother education below primary/ illiterate versus above primary. (F) Walking barefoot versus walking with footwear. (G) Recent deworming negative to recent deworming done. (H) Nails untrimmed versus trimmed. (I) Flooring earthen versus cemented. (J) Religion: Hindu versus other religions. (K) Poor hand wash habits versus good hand wash. CI, confidence interval; OR, odds ratio.
Table 2 Risk factors associated with STH
Variables Number of articles Odds ratio (95% CI) I2 (%); p-value
Males vs. females 10 1.14 (0.88–1.46) 78; 0.001
Open latrine vs. sanitary latrine 7 5.2 (1.35–20.16) 97.9; 0.001
Hand washing after defecation with water only vs. with soap and water 6 2.49 (1.51–4.12) 92.3; 0.001
SES lower vs. SES upper and middle 4 1.01 (0.74–1.38) 41.1; 0.165
Mother education below primary/illiterate vs. above primary 4 1.07 (0.77–1.47) 72.6; 0.012
Walking barefoot vs. walking with footwear 4 1.73 (0.92–3.28) 61.1; 0.052
Recent deworming negative to recent deworming done 4 1.41 (0.87–2.28) 72.1; 0.013
Nails untrimmed vs. trimmed 3 1.52 (0.43–5.45) 82.5; 0.003
Flooring earthen vs. cemented 3 2.02 (1.33–3.06) 60.2; 0.08
Religion: Hindu vs. other religions 3 1.27 (0.65–2.47) 82.2; 0.004
Poor hand wash habits vs. good hand wash 3 1.55 (0.61–3.92) 92.1; 0.001

Abbreviations: CI, confidence interval; SES, socioeconomic status; STH, soil-transmitted helminths.

Discussion

STH infections are common cause of morbidity in children of developing countries like India. According to the World Health Organization, around 24% of world population is infected with STH. Two-hundred and forty-one million children between the ages of 1 and 14 years are at risk of parasitic intestinal worms in India. This study covers all the published literature on STH, covering studies from all parts of India in pediatric population (0—18 years). Prevalence percentage of STH is a major determinant of routine deworming practices in a geographical area. The National Deworming Day is an initiative of Ministry of Health and Family Welfare, Government of India to make every child in the country worm-free. It is a large-scale public health program reaching huge number of children in a short period of time. Deworming twice a year is recommended in the states with prevalence of STH more than 20% and once a year in other states with less than 20% prevalence. Calculation of pooled prevalence of STH in pediatric population in different geographical areas of India obtained in this study will help in better implementation of such deworming practices.

In our study among the three STH, AL was most prevalent. A meta-analysis from South America showed a similar overall high burden of ascariasis.[53] In contrast, in a meta-analysis study from sub-Saharan Africa, HW was found to be the commonest STH infection.[54] In a systematic review published in 2016, the prevalence of AL, Ancylostoma duodenale and TT in 18 selected studies in India was in range between 0.4 and 71.87%, 0.14 and 42%, and 0.3 and 29.57%, respectively.[55] In our study, the prevalence of AL ranged from 0.8[18] to 91%[11] with a pooled prevalence of 25%. For TT, the prevalence ranged from 0.3[12] to 72%[11] with a pooled prevalence of 13%. For HW, the prevalence ranged from 0.2[13] to 80%[14] with pooled prevalence of 10%. Another review was from India by Salam et al 2017,[56] which aimed to understand the spatial distribution and identify the high-risk zones in India. They included 39 studies from all over India estimating the prevalence of AL infection in the range of 0.6 to 91%, TT in the ranged of 0.7 to 72% and HW ranging from 0.02 to 52%. Our study showed similar results except for HW that ranged from 0.2[13] to 80%,[14] higher than that reported by Salam et al. However, the previous studies[55] were done on all age groups as compared to ours that included pediatric population only, which is a better representative of disease burden in more susceptible population at risk.

Our analysis included studies from 20 states/union territories (UT) from India; however, some areas were completely missed due to lack of published literature from those regions. It would be helpful if all the states/UT have their own data to have even more accurate estimate of overall prevalence in those regions as well as India as a whole. Maximum number of studies were from North India and South India. The study selection and data extraction might cause bias in calculation of STH because of this. We tried to include as many studies as possible; however, some of them had to be excluded due to unavailability of full texts. Also, to obtain the prevalence, only community-based studies were selected including subjects who did not have any symptom related to STH. The hospital based or intervention studies were excluded to remove the bias since the symptomatic individuals or those with a previous diagnosis could not be included. The search strategy was very broad and included broad search query terms. For all the studies that did not report the presence of a particular helminth in an area, it was not clear whether it was not seen in their population or whether they did not look for it. This might have led to under reporting of the prevalence of individual helminths in those cases.

Regional variation in prevalence of the three organisms was seen. Local factors can play a role in their epidemiology. Our study gave results similar to the previous data and studies; Western India has the lowest prevalence of all three STH.[55,56] Pooled prevalence from northern and northeastern India for AL is higher as compared to other two organisms, whereas southern India had higher prevalence for TT. Eastern India had higher prevalence of HW. However, very high heterogeneity between studies as shown by higher I2 values restricts us from making conclusive remarks regarding this epidemiology. Overall, prevalence of STH (AL = 25%, TT = 13%, AD = 10%) as found in our study was comparable to other studies in different part of world.[57] The tropical and subtropical warm climate with humid environment in India provides ideal environment for the survival of parasitic eggs in moist soils. Besides, higher prevalence of STH in regions that are not hot and moist like Jammu and Kashmir[26-33] points towards role of other factors than climate including socioeconomic and behavioral factors. The unhealthy sociobehavioral habits due to poverty and poor personal and environmental hygiene, underlying socioeconomic factors, underdeveloped sanitation, lack of adequate water supply, increasing population, illiteracy, and poor sociobehavioral habits, and a large section of people living below poverty line play a role in spread of infections as seen from many studies. This meta-analysis includes data from children only as compared to previous studies that had diverse study population including children and adults both. Children in particular are more prone to these infections due to direct contact with soil while playing, poor hygiene, habits of playing or handling of contaminated soils, eating with soiled hands, unhygienic toilet practices, drinking and eating of contaminated water and food, and illiteracy of the care giver or mother. These specific risk factor for children makes them more susceptible to get STH infections that is a major cause of morbidity in pediatric age group. Cumulative OR of the risk factors from different studies calculated in our study would help in designing a better preventive care at different levels. Also, a superior assessment of the risk factors of STH would require meticulous country-specific data, preferably from nationally representative epidemiological surveys in various communities and geographical areas.

Two risk factors with higher OR were open defecation practices or open latrine (OR: 5.2) and washing hands without soap using water only (OR: 2.49) also point towards poor sanitation services as well as behavior related factors that play a very important role in STH infection in pediatric population. Earthen flooring with OR of 2.2 and walking barefoot with OR 1.73 are also an important risk factor for STH. Other risk factors studied, including sex predisposition (OR: 1.14), economic status (1.01), and mother's education (1.07), were not found to be significantly associated with STH. However, education of parents specially the mother or the caregiver is important in terms of general awareness and knowledge of following hygienic practices. Though pica[19] and anemia[24] were two risk factors studied in one study only, they had very high odds of having STH.

The prevalence and estimate of STH burden also depend on the diagnostic method used for the assessment.[58] Kato-Katz method has been described as the best method by the WHO as reliable diagnostic tool with better efficacy, accuracy, and predictive value than other techniques in resource poor settings. Only 7 out of 44 studies (16%) used Kato-Katz method for detection. Most studies relied upon direct microscopy and concentration techniques as preferred method. Using standard procedure for parasite detection can further increase the sensitivity of studies and help in better understanding of problem. Most of the studies performed only one stool examination, which may result in underreporting of the prevalence. Prevalence and intensity of STH infection are the only tool for preventive chemotherapy and to assess the effect of ongoing deworming program.

The control of STH comes with various challenges like improvement in sanitary conditions and accessibility to safe drinking water. These factors may reduce chances of infection or reinfection, hence decreasing the morbidity in children caused due to STH. In resource-poor settings, educating the people regarding healthy and hygienic practices, implementation, and expansion of mass deworming intervention to all the children can prove to be very effective. Targeting the teachers and caregivers of children for educating the kids about STH, motivating them for a behavioral change and adopting healthy practices such as washing hands with soap and water before handling food products and after using toilet, wearing protective footwear, thorough washing of raw vegetables and fruits with water before eating and sanitary disposal of human excreta can be very useful. These may further amplify the control measures and help to cut down STH transmission.

Conclusion

In our study, we tried to estimate the prevalence of STH in children by analyzing 44 studies from different regions in India. The studies differed from each other due to their heterogeneous sample size, study population, methods used to select, identify parasites, and also the parasites included by them. The pooled prevalence obtained for AL, TT, and HW in India in pediatric population is 25, 13, and 10%, respectively. The risk factors for STH were analyzed. This study may be useful for prevention and control strategies that will help the plan makers to concentrate on the high-risk groups at areas with high prevalence. Also, effective strategies can be designed keeping the most important risk factors in mind.

Authors' Contributions

P.C. and S.S. conceptualized the study. P.C. and S.S. contributed to data extraction. P.C., S.S., and S.P. did formal analysis. P.C., S.S., and V.K.D. were involved in supervision. P.C. and S.S. wrote the original draft. P.C., S.S., V.K.D., and S.P. were involved in writing, review, and editing. P.C., S.S., V.K.D., and S.P. gave approval of final version. All authors read and approved the final manuscript.

Availability of Data and Materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflict of Interest

None declared.

Funding

None.

References

  1. . Accessed June 12, 2022 from: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections
  2. , . The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors. 2012;5(01):81.
    [CrossRef] [PubMed] [Google Scholar]
  3. , , , . Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7(01):37.
    [CrossRef] [PubMed] [Google Scholar]
  4. . Accessed June 12, 2022 from: http://www.thiswormyworld.org/worms/global-burden
  5. , , , . PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(07):e1000097.
    [CrossRef] [PubMed] [Google Scholar]
  6. , , , et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008-2012.
    [CrossRef] [PubMed] [Google Scholar]
  7. , , . Development of a quality assessment tool for systematic reviews of observational studies (QATSO) of HIV prevalence in men having sex with men and associated risk behaviours. Emerg Themes Epidemiol. 2008;5:23.
    [CrossRef] [PubMed] [Google Scholar]
  8. , , , et al. Compliance to spectacle use in children with refractive errors- a systematic review and meta-analysis. BMC Ophthalmol. 2020;20(01):71.
    [CrossRef] [PubMed] [Google Scholar]
  9. , , , , , . Prevalence of soil-transmitted helminth infestations among children attending integrated child development service centers in a tea garden area in Darjeeling. Trop Parasitol. 2019;9(01):23-29.
    [Google Scholar]
  10. , , , et al. High prevalence of soil-transmitted helminth infections among primary school children, Uttar Pradesh, India, 2015. Infect Dis Poverty. 2017;6(01):139.
    [CrossRef] [PubMed] [Google Scholar]
  11. , , . Prevalence, intensity and risk factors for soil-transmitted helminth infection in a South Indian fishing village. Acta Trop. 2004;91(02):177-187.
    [CrossRef] [PubMed] [Google Scholar]
  12. , . Study on the prevalence of intestinal parasitic infections and the assessment of the efficacy of albendazole in soil-transmitted helminths in school-going children in East Sikkim. Trop Parasitol. 2020;10(01):18-23.
    [Google Scholar]
  13. , , . Prevalence and the factors influencing soil-transmitted helminths among school age children (5-14 years age) in a rural area of Coimbatore district. Trop Parasitol. 2020;10(02):74-78.
    [CrossRef] [PubMed] [Google Scholar]
  14. , , . The prevalence of intestinal helminths in religious groups of a rural community near Calcutta. Am J Epidemiol. 1968;87(02):313-317.
    [CrossRef] [PubMed] [Google Scholar]
  15. . Burden of ascariasis in schoolchildren of Assam. J Commun Dis. 2009;41(04):289-292.
    [Google Scholar]
  16. , , , et al. The epidemiology of soil-transmitted helminths in Bihar State, India. PLoS Negl Trop Dis. 2015;9(05):e0003790.
    [CrossRef] [PubMed] [Google Scholar]
  17. , , , , . Soil transmitted helminth infections among school going age children of slums from Bhubaneswar, Odisha. Trop Parasitol. 2020;10(01):34-38.
    [Google Scholar]
  18. , , , , . Intestinal parasitic infestation in school going children of Rishikesh, Uttarakhand, India. Indian J Community Health. 2018;30(01):45-50.
    [CrossRef] [Google Scholar]
  19. , , , , . Prevalence and risk factors of soil-transmitted helminth infections in school age children (6-14 years): a cross-sectional study in an urban resettlement colony of Delhi. Indian J Public Health. 2020;64(04):333-338.
    [CrossRef] [PubMed] [Google Scholar]
  20. , , . The prevalence of intestinal parasitic infections in the urban slums of a city in Western India. J Infect Public Health. 2013;6(02):142-149.
    [CrossRef] [PubMed] [Google Scholar]
  21. , , , , . Helminthic infections in school children in Puducherry, South India. J Microbiol Immunol Infect. 2010;43(03):228-232.
    [CrossRef] [PubMed] [Google Scholar]
  22. , , . Prevalence of intestinal parasitic infections among school children in rural area of Vizianagaram. IOSR J Pharm Biol Sci. 2012;11:42-44.
    [CrossRef] [Google Scholar]
  23. , , , , , . Prevalence and risk factors associated with worm infestation in pre-school children (6-23 months) in selected blocks of Uttar Pradesh and Jharkhand, India. Indian J Med Sci. 2008;62(12):484-491.
    [CrossRef] [PubMed] [Google Scholar]
  24. . An analytical study of factors related to infestation by intestinal parasites in rural school children (report of a pilot study) Public Health. 1979;93(02):82-88.
    [CrossRef] [PubMed] [Google Scholar]
  25. , , . Prevalence of Trichuris trichiura in relation to socio-economic & behavioural determinants of exposure to infection in rural Assam. Indian J Med Res. 2000;112:140-146.
    [Google Scholar]
  26. , . Intestinal helminths and associated risk factors in children of district Pulwama, Kashmir, India. Indian J Med Microbiol. 2009;27(01):81-82.
    [CrossRef] [PubMed] [Google Scholar]
  27. , . Intestinal helminth infections among children of district Shopian of Kashmir Valley, India. J Parasit Dis. 2016;40(04):1422-1425.
    [CrossRef] [PubMed] [Google Scholar]
  28. , , , et al. Soil-transmitted helminths in relation to hemoglobin status among school children of the Kashmir Valley. J Parasitol. 2008;94(03):591-593.
    [CrossRef] [PubMed] [Google Scholar]
  29. , , . Recent patterns and risk factors of intestinal helminthes infection among school children in Kashmir, India. Arch Clin Microbiol. 2011;2(03):1-4.
    [Google Scholar]
  30. , , , , , . Prevalence of intestinal parasites and associated risk factors among schoolchildren in Srinagar City, Kashmir, India. J Parasitol. 2007;93(06):1541-1543.
    [CrossRef] [PubMed] [Google Scholar]
  31. , , , , , . Intestinal helminths in a population of children from the Kashmir valley, India. J Helminthol. 2008;82(04):313-317.
    [CrossRef] [PubMed] [Google Scholar]
  32. , , , , , . Intestinal helminthiasis in children of Gurez valley of Jammu and Kashmir state, India. J Glob Infect Dis. 2010;2(02):91-94.
    [CrossRef] [PubMed] [Google Scholar]
  33. , , , , , . Helminthic infestation in children of Kupwara district: a prospective study. Indian J Med Microbiol. 2007;25(04):398-400.
    [CrossRef] [PubMed] [Google Scholar]
  34. , , . Population biology of hookworms in children in rural West Bengal. I. General parasitological observations. Am J Trop Med Hyg. 1978;27(06):1152-1161.
    [CrossRef] [PubMed] [Google Scholar]
  35. , , , , . Soil transmitted helminths prevalence in school children of Pauri Garhwal District, Uttaranchal state. J Commun Dis. 2006;38(01):112-114.
    [Google Scholar]
  36. , . S A. Prevalence of malnutrition and intestinal parasites in preschool slum children in Lucknow. Indian Pediatr. 1997;34(07):599-605.
    [Google Scholar]
  37. , , . Intestinal parasitic infestation among children in a semi-urban Indian population. Trop Parasitol. 2011;1(02):104-107.
    [CrossRef] [PubMed] [Google Scholar]
  38. , . Prevalence of parasitic infections among school children in Bhaili, Durg, Chhattisgarh. Int J Curr Microbiol Appl Sci. 2018;7(09):1919-1925.
    [CrossRef] [Google Scholar]
  39. , , . Prevalence and risk factors associated with the presence of Soil-Transmitted Helminths in children studying in Municipal Corporation of Delhi Schools of Delhi, India. J Parasit Dis. 2015;39(03):377-384.
    [CrossRef] [PubMed] [Google Scholar]
  40. . Epidemiology of gastroenteritis of pre-school children in slum areas in Delhi with reference to helminthic and parasitic infection. Indian J Pediatr. 1978;45(369):303-309.
    [CrossRef] [PubMed] [Google Scholar]
  41. , , , et al. Association between the socioeconomic determinants and soil-transmitted helminthiasis among school-going children in a rural area of Haryana. J Family Med Prim Care. 2020;9(07):3712-3715.
    [CrossRef] [PubMed] [Google Scholar]
  42. , , , . Intestinal Parasitic infections and Demographic status of school children in Bhopal region of Central India. IOSR Journal of Pharmacy and Biological Sciences. 2014;9(05):83-87.
    [CrossRef] [Google Scholar]
  43. , , , . Intestinal parasitic infection in Bhil tribe of Rajasthan, India. J Parasit Dis. 2012;36(02):143-148.
    [CrossRef] [PubMed] [Google Scholar]
  44. , , , . Intestinal parasitic infestations among school children in Piparia Village, Vadodara District. Int J Sci Res. 2012;2:434-436.
    [CrossRef] [Google Scholar]
  45. , , . Intestinal helminth infections among school children in Visakhapatnam. Indian J Pediatr. 1999;66(05):669-673.
    [CrossRef] [PubMed] [Google Scholar]
  46. , , , . Prevalence of Intestinal Parasitic Infection in School Going Children in Amalapuram, Andhra Pradesh, India. Shiraz E Med J. 2013;14(04):e16652.
    [CrossRef] [Google Scholar]
  47. , . Prevalence of intestinal parasites in school going children in a rural community. Int J Biomed Res. 2011;2(12):605-607.
    [CrossRef] [Google Scholar]
  48. , , , . Prevalence and distribution of soil transmitted helminths (STH) among asymptomatic school going children in South Chennai, Tamil Nadu, India. Int J Med Public Health. 2011;1(02):57-59.
    [CrossRef] [Google Scholar]
  49. . A survey of intestinal helminths among children of different social communities in Madras, India. Trans R Soc Trop Med Hyg. 1984;78(01):132-133.
    [CrossRef] [PubMed] [Google Scholar]
  50. , , , et al. Prevalence & risk factors for soil transmitted helminth infection among school children in south India. Indian J Med Res. 2014;139(01):76-82.
    [Google Scholar]
  51. , , , . Intestinal parasitic infestations and anemia among urban female school children in Kancheepuram district, Tamil Nadu. J Family Med Prim Care. 2018;7(06):1395-1400.
    [CrossRef] [PubMed] [Google Scholar]
  52. . Prevalence of parasitic infections among primary school children in Bangalore. International Journal of Basic and Applied Sciences. 2014;4(01):356-361.
    [Google Scholar]
  53. , , , , , . Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2013;13(06):507-518.
    [CrossRef] [PubMed] [Google Scholar]
  54. , , , et al. Spatial and temporal distribution of soil-transmitted helminth infection in sub-Saharan Africa: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2015;15(01):74-84.
    [CrossRef] [PubMed] [Google Scholar]
  55. , , , , , . Prevalence of soil-transmitted helminthic infection in India in current scenario: a systematic review. J Commun Dis. 2016;48(02):24-35.
    [Google Scholar]
  56. , . Prevalence and distribution of soil-transmitted helminth infections in India. BMC Public Health. 2017;17(01):201.
    [CrossRef] [PubMed] [Google Scholar]
  57. , , . The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PLoS Negl Trop Dis. 2010;4(07):e779.
    [CrossRef] [PubMed] [Google Scholar]
  58. . Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers–a review. Int J Parasitol. 2010;40(10):1137-1144.
    [CrossRef] [PubMed] [Google Scholar]
Show Sections