Hrev_master Healthcare in Low-resource Settings 2023; volume 11:11742 The impact of soil-transmitted helminths infection on growth impair- ment: systematic review and meta analysis James Hadiputra Sunarpo, Kartika Ishartadiati, Andra Agnez Al Aska, Sukma Sahadewa, Ayling Sanjaya Faculty of Medicine, Universitas Wijaya Kusuma Surabaya, Surabaya, Indonesia Abstract Human helminthiasis, particularly soil-transmitted helminth (STH) infections, is a prevalent health concern in Indonesia, espe- cially among children, often resulting in growth disorders, notably stunting. To examine the link between STH infections and child- hood stunting, we conducted a comprehensive review of literature spanning 2012-2023, encompassing 40 selected articles from databases like Pubmed, Science Direct, and Google Scholar. Our analysis revealed a substantial association between STH infec- tions and increased stunting risk in children, estimating a 44.407% rise in stunting risk due to STH infection. Stunting, a consequence of chronic malnutrition, profoundly affects a child’s physical and cognitive development, with long-lasting repercussions on their future potential and quality of life. This study has significant implications. It underscores the urgent need for robust public health interventions targeting STH infections, especially in high- prevalence areas like Indonesia. Measures such as mass deworm- ing campaigns, improved sanitation and hygiene practices, and health education can significantly alleviate the burden of STH infections and the resulting stunting. Moreover, the research emphasizes the intricate relationship between infectious diseases and malnutrition, highlighting the necessity for a holistic approach to child health. Addressing STH infections necessitates not only medical intervention but also efforts to enhance overall living con- ditions and nutritional status. Integrating these approaches into a comprehensive public health strategy can yield more effective and sustainable results in the fight against childhood stunting. In con- clusion, this study underscores the paramount importance of addressing STH infections in the context of child growth and underscores the urgency of implementing effective public health interventions. This approach can enable children to reach their full physical and cognitive potential, ultimately contributing to the overall well-being and development of societies. Introduction Human helminthiasis, caused by parasitic worms, is a widespread issue.1 In Indonesia, Soil-Transmitted Helminths (STH) are the most common type. Globally, over 2 billion people have STH infections, with 300 million experiencing severe cases, resulting in 150,000 deaths. Ascaris lumbricoides affects about 1.2 billion, Ancylostoma duodenale and Necator americanus impact 740 million, and Trichuris trichiura affects around 795 million people.2,3 Indonesia ranks second worldwide in STH infections, primarily affecting preschool-age children. Severely endemic provinces include Banten, DKI Jakarta, South Sulawesi, Bali, Papua, and Nusa Tenggara due to the favorable tropical climate and poor sanitation.4–6 East Java reports an approximately 80.69% prevalence rate, with Surabaya City noting 36% in 2015 according to the Ministry of Health of the Republic of Indonesia.7,8 STH are frequently found in preschool and school-aged chil- dren with poor hand hygiene and sanitation practices, making it easier for STH to enter their bodies and disrupt their growth and development processes.4,5 Growth and developmental disorders commonly observed in children include stunting.9,10 Stunting is a growth and developmental disorder in children caused by factors such as malnutrition, repeated infections, and insufficient psy- chosocial stimulation.11–14 In Indonesia, the incidence of stunting is alarmingly high, affecting around 7 million toddlers. In East Java province, the stunting incidence is approximately 32%.15,16 The consequences of stunting include increased morbidity, mortal- ity, suboptimal cognitive and motor development, decreased reproductive capacity, suboptimal learning ability at school, and reduced work productivity.17–19 Correspondence: Kartika Ishartadiati, Faculty of Medicine, Universitas Wijaya Kusuma Surabaya, Surabaya, Indonesia. E-mail: kartika.ishartadiati@uwks.ac.id Key words: soil-transmitted helminths; helminthiasis; stunting; early childhood development. Contributions: JHS, Conceptualization, Paper Identification, Selection, Abstraction, Analysis, Methodology, Writing – Original Draft, Review and Editing; KI, Conceptualization, Methodology, Validation, Writing – Original Draft, Review and Editing; AAAA, Validation, Review and Editing; SS Validation, Review and Editing; AS, Review and Editing. Conflict of interest: the authors declare no conflict of interest. Funding: this research did not receive external funding. Acknowledgements: we would like to thankful to the database providers PubMed, Science Direct, and Google Scholar for their valuable contributions to this study. Received: 10 September 2023. Accepted: 25 October 2023. Early access: 9 November 2023. This work is licensed under a Creative Commons Attribution 4.0 License (by-nc 4.0). ©Copyright: the Author(s), 2023 Licensee PAGEPress, Italy Healthcare in Low-resource Settings 2023; 11:11742 doi:10.4081/hls.2023.11742 Publisher's note: all claims expressed in this article are solely those of the authors and do not necessarily represent those of their affili- ated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher. [page 64] [Healthcare in Low-resource Settings 2023; 11:11742] Non -co mmerc ial us e o nly The rate of STH infection in stunted children under 5 years old is estimated at 30.43%, with Ascaris lumbricoides and Trichuris trichiura being the primary causes of infection. Several factors may contribute to the incidence of STH infections in toddlers, including their medical history, frequency of illnesses in the preceding three months, stunting issues, and their cleanliness and hygiene habits (e.g., handwashing with soap before eating and after using the toi- let).17–19 In recent years, research on STH infections and stunting has expanded worldwide, with some studies indicating a signifi- cant relationship and others suggesting no significant connection between STH infection and stunting in children.20–22 Therefore, this study was conducted to investigate the incidence of STH infection and stunting in children, as well as to explore the relationship between these two factors. The research aims to provide up-to-date information with a reasonably high level of accuracy. The researcher conducted a systematic literature review and meta-anal- ysis to examine the relationship between Soil-Transmitted Helminths infection and the incidence of stunting in children. It is hoped that this research will offer insights for the prevention and treatment of STH infections and stunting in accordance with the goals of the government of the Republic of Indonesia in 2024 and the SDGs target in 2030. This study aims to establish the relation- ship between STH infection and the incidence of stunting in chil- dren through a systematic review and meta-analysis approach. Materials and Methods Design study This study employed systematic literature review and meta- analysis methods. Articles were systematically and comprehen- sively searched across various databases, including PubMed, ScienceDirect, and Google Scholar, covering publications from 2012 to 2023. The article search was conducted over approximate- ly 5 months. The search terms used were as follows: STH infec- tions* and stunting; STH infections* and stunted; STH infections* and growth disorders; helminthiasis* and stunting; helminthiasis* and stunted; helminthiasis* and growth disorders (where * indi- cates truncation). Population and sample Eligibility criteria were established to select studies for inclu- sion in the systematic literature review or meta-analysis. The pop- ulation of interest in this study was children. The intervention under investigation was Soil-Transmitted Helminths (STH) infec- tion, and the primary outcome of interest was stunting. Inclusion criteria for research articles were as follows: studies investigating the relationship between Soil-Transmitted Helminths infection and the incidence of stunting in children, research articles published between 2012 and 2023, research articles available in Indonesian and English, and research articles with clearly defined methodolo- gies. Exclusion criteria encompassed incomplete research manuscripts, research results inaccessible for completeness, research lacking both qualitative and quantitative results, and research publications in the form of commentary or opinion pieces. Operational definition of variables STH infection refers to intestinal nematode infections affecting humans, where transmission occurs through contact with soil con- taminated by eggs or larvae of STH worms. These STH worms include Ascaris lumbricoides, Necator Americanus, Ancylostoma duodenale, Trichuris trichiura, and Strongyloides stercoralis. Stunting is a developmental disorder primarily caused by malnutri- tion, recurrent infections, and insufficient psychosocial stimulation. Data analysis Data processing involved the use of MedCalc Software, which calculated heterogeneity and performed Egger’s test to determine the model of studies to be combined and to derive the final results of the meta-analysis. Results The selected articles encompassed publications from both international and national journals. Supplementary Material Table 1 and Table 1 provides an overview of the articles that met the inclu- sion criteria. Article summary A total of forty (40) articles were deemed suitable for inclusion in the meta-analysis focusing on the relationship between Soil- Transmitted Helminths infection and the incidence of stunting in children. During the initial search process, a total of 1,157 articles were identified. These articles were subsequently subjected to a screening process, during which 150 articles were assessed for rel- evance and full-text availability in accordance with the predeter- mined inclusion and exclusion criteria. Ultimately, 40 articles, which specifically addressed the relationship between STH infec- tion and the incidence of stunting in children, successfully passed the screening phase and satisfied the established inclusion and exclusion criteria. As such, these 40 articles were included in the systematic literature review and meta-analysis (Figure 1). Transforming Healthcare in Low-Resource Settings: a Multidisciplinary Approach Towards Sustainable Solutions Figure 1. Prisma diagram of the review process. [Healthcare in Low-resource Settings 2023; 11:11742] [page 65] Non -co mmerc ial us e o nly Meta-analysis article Forest plot Table 2 demonstrates a considerable degree of variation between studies, as evident by the p-value in the heterogeneity test being less than 0.05, specifically p < 0.0001, and a high I2 value of 98.02%. Therefore, the results in the meta-analysis were analyzed using the total fixed-effects model. The forest plot in Figure 2 illus- trates that the proportion obtained is 47.642% (95% CI 47.179 - 48.105). Consequently, it can be concluded that STH infection increases the risk of stunting in children by a factor of 47.462. Funnel plot To identify the presence of publication bias in this study, fun- nel plots and Egger’s test were employed. In Figure 3, the funnel plot indicates an asymmetrical distribution of studies, as it is not [page 66] [Healthcare in Low-resource Settings 2023; 11:11742] Transforming Healthcare in Low-Resource Settings: a Multidisciplinary Approach Towards Sustainable Solutions Table 1. Meta-analysis of the articles used. Study Sample size Proportion (%) 95% CI Weight (%) Fixed Random Wirjanata 2023 622 80.386 77.044 to 83.436 1.39 2.71 Manga 2023 350 38.286 33.169 to 43.603 0.78 2.66 Nasution 2022 46 58.696 43.227 to 73.003 0.10 2.08 Dehury 2022 232 32.759 26.759 to 39.205 0.52 2.61 Olin 2022 230 68.696 62.272 to 74.630 0.51 2.60 Ickowitz 2022 422 50.474 45.596 to 55.345 0.94 2.68 Hlaing 2022 264 32.576 26.957 to 38.591 0.59 2.63 Kassa 2022 405 39.753 34.954 to 44.703 0.90 2.68 Heffernan 2022 80 15.000 7.998 to 24.736 0.18 2.33 Yeshanew 2022 392 51.020 45.953 to 56.073 0.87 2.67 Diptyanusa 2022 138 51.449 42.797 to 60.038 0.31 2.50 Nuraini 2022 60 60.000 46.541 to 72.438 0.14 2.21 Degarege 2022 1205 44.149 41.321 to 47.006 2.68 2.75 Manggabarani 2022 209 47.368 40.440 to 54.373 0.47 2.59 Yogaswara 2022 185 40.000 32.882 to 47.443 0.41 2.56 Munfiah 2021 51 52.941 38.459 to 67.070 0.12 2.13 Lim 2021 343 39.942 34.719 to 45.339 0.77 2.66 Demonteverde 2021 1689 35.406 33.122 to 37.740 3.76 2.76 Shaqti 2021 160 35.000 27.639 to 42.928 0.36 2.53 Hasanuddin 2021 20 10.000 1.235 to 31.698 0.047 1.59 Fernandez 2021 100 42.000 32.199 to 52.288 0.22 2.41 Morrisey 2021 380 47.895 42.774 to 53.049 0.85 2.67 Tumwesigire 2021 206 79.126 72.931 to 84.462 0.46 2.59 Salimo 2020 200 27.000 20.980 to 33.715 0.45 2.58 Chelkeba 2020 404 27.970 23.645 to 32.622 0.90 2.68 Hailegebriel 2020 24716 44.999 44.378 to 45.622 55.02 2.78 Augustina 2020 47 57.447 42.178 to 71.742 0.11 2.09 Beyene 2020 622 59.325 55.347 to 63.213 1.39 2.71 Sihombing 2020 2179 41.854 39.772 to 43.958 4.85 2.76 Mbonigaba 2020 4998 66.967 65.643 to 68.271 11.13 2.77 Nathasaria 2020 80 1.250 0.0316 to 6.769 0.18 2.33 Swastika 2019 81 25.926 16.820 to 36.860 0.18 2.33 Angraini 2019 40 47.500 31.512 to 63.872 0.091 2.01 Magga 2019 26 46.154 26.587 to 66.629 0.060 1.76 Moncayo 2018 920 56.957 53.685 to 60.184 2.05 2.74 Campbell 2017 2038 45.535 43.356 to 47.727 4.54 2.76 Teshome 2017 148 59.459 51.088 to 67.444 0.33 2.52 Alexandra 2017 80 21.250 12.894 to 31.829 0.18 2.33 Muhoho 2016 236 59.746 53.187 to 66.057 0.53 2.61 Sembiring 2015 281 35.587 29.990 to 41.492 0.63 2.63 Total (fixed effects) 44885 47.642 47.179 to 48.105 100.00 100.00 Total (random effects) 44885 44.407 40.341 to 48.510 100.00 100.00 Non -co mmerc ial us e o nly balanced on both sides of the central line boundary. This suggests that publication bias affects the relationship between STH infec- tion and the incidence of stunting in children. Furthermore, the publication bias test using Egger’s test, as presented in Table 3, reveals that the intercept value is not equal to zero, specifically - 0.6427. Based on the results of Egger’s test, it is evident that pub- lication bias influences the relationship between STH infection and the incidence of stunting in children. Discussion The results of the meta-analysis involving 40 articles examin- ing the relationship between STH infection and the incidence of stunting in children were synthesized in a forest plot. Figure 2 in the forest plot indicates that children with STH infection face a risk increase of approximately 44.407%. In a study conducted by Demonteverde (2021), it was revealed that STH infection had a significant association with the incidence of stunting in children. This research employed a systematic literature review approach, focusing on Filipino schoolchildren. The findings of this study suggest that STH infection can lead to structural changes in the intestines, resulting in reduced villi function and a decreased num- ber of immune cells that protect the intestines. This, in turn, can hinder the absorption of essential nutrients crucial for child growth and development.38 Another study conducted by Hailegebriel (2020) highlighted the impact of STH infection on growth and development disorders in children, including stunting. This systematic review and meta- analysis centered on school-age children or children under 10 years old in Ethiopia. The study emphasized external factors such as poor environmental sanitation, inadequate hand hygiene, unclean drinking water, and insufficient family education as con- tributors to stunting.46 Additionally, a study by Campbell (2017) identified the influ- ence of STH infection on impaired growth and development in children, specifically leading to stunting. The research explored the connection between STH infections, hemoglobin levels, and child development indices in Manufahi District, Timor-Leste. The findings revealed that children with STH infection were twice as likely to experience stunting compared to their unaffected peers.55 Mbonigaba’s study (2020) showed a significant association between STH infection and the incidence of stunting in children. Using Kato Katz microscopy (KK) and real-time PCR (qPCR) techniques to analyze 4998 children in Western Rwanda, the study indicated that around 88% of Rwandan children were affected by Soil-Transmitted Helminths infection, along with other conditions like stunting.50 Similarly, Sihombing’s study (2020) found that STH infection influenced impaired nutritional status and cognitive ability in chil- dren. This research explored the relationship between STH infec- tion, nutritional status, and cognitive ability in children in Indonesia, revealing that children with STH infection were more vulnerable to stunting compared to those without.49 While this study offers valuable insights, it is important to acknowledge several limitations. The quality of the meta-analysis and systematic review depends on the quality of the source articles. Variability in data quality and reporting standards across the select- ed articles may introduce bias and uncertainty into the results. The study focused on articles published from 2012 to 2023, which may not fully capture the historical and geographical variations in STH infection and stunting prevalence. These factors can change over time and may vary in different regions. Additionally, the study may be subject to language bias, as it relied on articles available in Transforming Healthcare in Low-Resource Settings: a Multidisciplinary Approach Towards Sustainable Solutions Table 2. Test of heterogeneity of the association of STH infection with the incidence of stunting in children. Q 1965.4566 DF 39 Significance level p<0.0001 I2 (inconsistency) 98.02% 95% CI for I2 97.71 to 98.28 Table 3. Publication bias test of the association of STH infection with the incidence of stunting in children. Egger's test Intercept -0.6427 95% CI -3.6784 to 2.3931 Significance level P = 0.6707 Figure 2. Forest plot of the relationship between Soil Transmitted Helminths (STH) infection and the incidence of stunting in chil- dren. Figure 3. Funnel plot of the association of Soil-Transmitted Helminths (STH) infection with the incidence of stunting in chil- dren. [Healthcare in Low-resource Settings 2023; 11:11742] [page 67] Non -co mmerc ial us e o nly Indonesian and English, potentially overlooking relevant research published in other languages. Addressing these limitations in future research will enhance our understanding of the relationship between Soil-Transmitted Helminths (STH) infections and stunt- ing, providing more accurate insights for policy development and intervention strategies. Conclusions S High STH infection rates in Indonesian children result from the tropical climate, poor sanitation, unhygienic water, and inade- quate education. STH infections, notably, lead to stunting, impair- ing child growth and development. This meta-analysis establishes that STH-infected children are at higher risk of stunting. This study contributes to the understanding of parasitic infections and growth impairment in pediatrics, parasitology, and public health. Practically, health professionals and policymakers must prioritize public health initiatives. Deworming programs, sanitation improvements, and health education are vital for countering STH infections and their adverse effects on children. On a governmental level, this research supports policies to reduce childhood STH infections. It offers a blueprint for regions with similar challenges, aiding in resource allocation to combat helminthiasis, thus enhanc- ing community health and well-being. References 1. Eyayu T, Yimer G, Workineh L, et al. Prevalence, intensity of infection and associated risk factors of soil-transmitted helminth infections among school children at Tachgayint woreda, Northcentral Ethiopia. PLoS One 2022;17:e0266333. 2. WHO. Soil-transmitted helminth infections. World Health Organization. 2023. 3. 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Paediatrica Indonesiana 2015;55:136-41. [page 70] [Healthcare in Low-resource Settings 2023; 11:11742] Transforming Healthcare in Low-Resource Settings: a Multidisciplinary Approach Towards Sustainable Solutions Online supplementary material: Table 1. Articles included in the meta-analysis. Non -co mmerc ial us e o nly