Risk Factor of Blastocystis hominis and Giardia duodenalis among Stunted Children in Bandung Regency, Indonesia
-
Nisa Fauziah
,
Ika Puspa Sari
,
Lia Faridah
,
Irvan Afriandi
,
Ryadi Adrizain
,
Naufal Fakhri Nugraha
,
Agnes Kurniawan
Abstract
Background: Stunting, resulting from chronic malnutrition, increases susceptibility to infections due to immature immunity. Blastocystis hominis and Giardia duodenalis may contribute to stunting. We aimed to determine the characteristics of intestinal protozoan infection among stunting children.
Methods: A cross-sectional study was conducted in 2020 among 280 stunted children in Bandung Regency, West Java, Indonesia. Faecal specimens were collected, with portions preserved separately in 10% formaldehyde and RNA Later solution. Of these, 230 met the examination criteria. Risk factors and demographic data were obtained through interviews. DNA was extracted, and intestinal protozoan infection were detected using PCR targeting the 18S SSU rRNA gene for B. hominis and 16S-like RNA gene for G. duodenalis.
Results: The prevalence of G. duodenalis and B. hominis was 5.6% (13/230) and 55.6% (128/230), respectively. Multivariate analysis identified age (P-value 0.004; OR 0.327) and no availability of a septic tank (P-value 0.021; OR 4.881) were the significant risk factors for G. duodenalis infection. For B. hominis infection, significant risk factors included age (P-value 0.033; OR 0.722) and gender (P-value 0.047; OR 1.742).
Conclusion: Stunting and intestinal protozoan infection present a dual burden. G. duodenalis and B. hominis infections were prevalent among stunted children. Significant risk factors included age and septic tank unavailability for G. duodenalis, while age and gender were associated with B. hominis infection. Improved sanitation and targeted interventions are essential to reduce infection risks.
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4. Sánchez A, Munoz M, Gómez N, et al. Molecular epidemiology of Giardia, Blastocystis and Cryptosporidium among indigenous children from the Colombian Amazon Basin. Front Microbiol. 2017;8:248.
5. Maryanti E, Lesmana SD, Mandela H. Deteksi Protozoa Usus Oportunistik pada Penderita Diare Anak di Puskesmas Rawat Inap Pekanbaru. Jurnal Ilmu Kedokteran. 2017;9(1):22–6.
6. Fauziah N, Aviani JK, Agrianfanny YN, et al. Intestinal Parasitic Infection and Nutritional Status in Children under Five Years Old: A Systematic Review. Trop Med Infect Dis. 2022;7(11):371.
7. Abou-Seri H, Abdalgaber M, Zahran F. Enteric parasitic infections: From environmental enteric dysfunction to gut microbiota and childhood malnutrition. Parasitologists United Journal. 2022;15(3):216–23.
8. Kotloff KL. The Burden and Etiology of Diarrheal Illness in Developing Countries. Pediatr Clin North Am. 2017;64(4):799–814.
9. Rojas-Velázquez L, Morán P, Serrano-Vázquez A, et al. The regulatory function of Blastocystis spp. on the immune inflammatory response in the gut microbiome. Front Cell Infect Microbiol. 2022;12:967724.
10. Bora I, Dutta V, Lyngdoh WV, et al. Study of intestinal parasites among the immunosuppressed patients attending a tertiary-care center in Northeast India. Int J Med Sci Pub Health. 2016;5(5):924–9.
11. Guerrant RL, DeBoer MD, Moore SR, et al. The impoverished gut—a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol. 2013; 10(4):220–9.
12. Vilcins D, Sly PD, Jagals P. Environmental risk factors associated with child stunting: a systematic review of the literature. Ann Glob Health. 2018;84(4):551-562.
13. Zavala GA, García OP, Camacho M, et al. Intestinal parasites: Associations with intestinal and systemic inflammation. Parasite Immunol. 2018;40(4): e12518.
14. Yoseph A, Beyene H. The high prevalence of intestinal parasitic infections is associated with stunting among children aged 6–59 months in Boricha Woreda, Southern Ethiopia: a cross-sectional study. BMC Public Health. 2020;20(1):1270.
15. Sardinha-Silva A, Alves-Ferreira EV, Grigg ME (2022). Intestinal immune responses to commensal and pathogenic protozoa. Front Immunol, 13:963723.
16. Mohammed J, Shiferaw A, Zeleke A, et al. Prevalence and Associated Risk Factors of Intestinal Parasites among Diarrheic Under-Five Children Attending Bahir Dar and Han Health Centers, Northwest Ethiopia: A Cross-Sectional Study. J Parasitol Res. 2022;2022: 7066529.
17. Badan Penelitian dan Pengembangan Kesehatan Kementerian Kesehatan Republik Indonesia. Riset Kesehatan Dasar 2018. Badan Penelitian dan Pengembangan Kesehatan Kementerian Kesehatan Republik Indonesia; 2018. https://repository.badankebijakan.kemkes.go.id/id/eprint/3514/1/Laporan%20Riskesdas%202018%20Nasional.pdf
18. Ayana M, Cools P, Mekonnen Z, et al. Comparison of four DNA extraction and three preservation protocols for the molecular detection and quantification of soil-transmitted helminths in stool. PLoS Negl Trop Dis. 2019;13(10):e0007778.
19. Mardani Kataki M, Tavalla M, Beiromvand M. Higher prevalence of Blastocystis hominis in healthy individuals than patients with gastrointestinal symptoms from Ahvaz, southwestern Iran. Comp Immunol Microbiol Infect Dis. 2019;65:160–4.
20. Costache C, Kalmár Z, Colosi HA, et al. First Multilocus Sequence Typing (MLST) of Giardia duodenalis Isolates from Humans in Romania. Parasit Vectors. 2020;13(1):387.
21. Hajissa K, Islam MA, Sanyang AM, et al. Prevalence of intestinal protozoan parasites among school children in Africa: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2022;16(2):e0009971.
22. Debash H, Alemu M, Bisetegn H. The prevalence of intestinal parasites, undernutrition and their associated risk factors among school-age children in Sekota Town, Northeast Ethiopia: A community-based cross-sectional study. Health Sci Rep. 2023;6(3):e1137.
23. Gabain IL, Ramsteijn AS, Webster JP. Parasites and Childhood Stunting – A Mechanistic Interplay with Nutrition, Anemia, Gut Health, Microbiota, and Epigenetics. Trends Parasitol. 2023;39(3):167–80.
24. Deka S, Kalita D, Hazarika N. Prevalence and Risk Factors of Intestinal Parasitic Infection in Under-Five Children with Malnutrition: A Hospital Based Cross-Sectional Study. J Family Med Prim Care. 2022;11(6):2794- 2801.
25. Gutiérrez-Jiménez J, Luna-Cázares LM, Martínez-de la Cruz L, et al. Children from a Rural Region in the Chiapas Highlands, Mexico, Show an Increased Risk of Stunting and Intestinal Parasitoses when Compared with Urban Children. Bol Med Hosp Infant Mex. 2019;76(1):18–26.
26. Wahdini S, Putra VP, Sungkar S. The Prevalence of Intestinal Protozoan Infections among Children in Southwest Sumba Based on the Type of Water Sources. Infect Chemother. 2021;53(3):519-527.
27. Rozi MF, Darlan DM, Rahmawati R, et al. Intestinal Parasitic Infections and Eosinophilia: A Cross-sectional Study among Primary School-aged Children in Medan, Indonesia. International Journal of Human and Health Sciences. 2020;4(4):277–81.
28. Cociancic P, Torrusio SE, Garraza M, et al. Intestinal Parasites in Child and Youth Populations of Argentina: Environmental Factors Determining Geographic Distribution. Rev Argent Microbiol. 2021;53(3):225–32.
29. Gozalbo M, Pavón A, Toledo R, et al. Epidemiological Study of Intestinal Parasitism in the Child Population of Department of Managua (Nicaragua). IJCMC. 2021;14(5):1–10.
30. Arshad S, Khatoon N, Warind JA, et al. The Prevalence of Human Intestinal Protozoal and Helminthic Infection in Karachi. Int J Biol Biotech. 2019;16(2):319–23.
31. Hussein JN, Meerkhan AA. The Incidence of Intestinal Parasites among Children in Hivi Pediatric Hospital, Duhok, Iraq. Science Journal of University of Zakho. 2019;7(1):1–4.
32. Khariri, Agtini MD, Ariyanti E, et al. Parasitic Infestation in the Incidence of Diarrhea among Toddlers in Jakarta, Bogor, Banjarmasin and Makassar. Proceedings of the 4th International Symposium on Health Research (ISHR 2019). 2020;658–62.
33. Yentur Doni N, Yildiz Zeyrek F, Simsek Z, et al. Risk Factors and Relationship Between Intestinal Parasites and the Growth Retardation and Psychomotor Development Delays of Children in Şanlıurfa, Turkey. Turkiye Parazitol Derg. 2015;39(4):270–6.
34. Ignatius R, Gahutu JB, Klotz C, et al. High Prevalence of Giardia duodenalis Assemblage B Infection and Association with Underweight in Rwandan Children. PLoS Negl Trop Dis. 2012;6(6):e1677.
35. Shaima SN, Das SK, Ahmed S, et al. Anthropometric Indices of Giardia-Infected Under-Five Children Presenting with Moderate-to-Severe Diarrhea and Their Healthy Community Controls: Data from the Global Enteric Multicenter Study. Children (Basel). 2021; 8(12):1186.
36. Afridi MF, Farhat K, Ali S, et al. Prevalence of Intestinal Parasitic Infestations in Relation to Wasting among Children Under 5 Years of Age in Skardu, Pakistan: A Cross-Sectional Observational Study. Isra Med J. 2021;13(2):130–3.
37. Fakhri Y, Daraei H, Ghaffari HR, et al. The risk factors for intestinal Giardia spp infection: Global systematic review and meta-analysis and meta-regression. Acta Trop. 2021; 220:105968.
38. Zonta ML, Cociancic P, Oyhenart EE, et al. Intestinal Parasitosis, Undernutrition and Socio-Environmental Factors in Schoolchildren from Clorinda Formosa, Argentina. Rev Salud Publica (Bogota). 2019; 21(2):224–31.
39. Kantzanou M, Karalexi MA, Vrioni G, et al. Prevalence of intestinal parasitic infections among children in Europe over the last five years. Trop Med Infect Dis. 2021;6(3):160.
40. Ghani MKA, Alharizi T. Blastocystosis amongst the Orang Asli (Aborigine) Schoolchildren at Pos Senderut, Kuala Lipis, Malaysia. Int Med J. 2021;28(2):217–9.
41. Deng Y, Zhang S, Ning C, et al. Molecular Epidemiology and Risk Factors of Blastocystis sp. Infections among General Populations in Yunnan Province, Southwestern China. Risk Manag Healthc Policy. 2020;13:1791-1801.
42. Athiyyah AF, Surono IS, Ranuh RG, et al. Mono-Parasitic and Poly-Parasitic Intestinal Infections among Children Aged 36–45 Months in East Nusa Tenggara, Indonesia. Trop Med Infect Dis. 2023;8(1):45.
2. Hajare ST, Gobena RK, Chauhan NM, Eriso F. Prevalence of Intestinal Parasite Infections and Their Associated Factors among Food Handlers Working in Selected Catering Establishments from Bule Hora, Ethiopia. Biomed Res Int. 2021;2021: 6669742.
3. Reh L, Muadica AS, Köster PC, et al. Substantial Prevalence of Enteroparasites Cryptosporidium spp., Giardia duodenalis and Blastocystis sp. In Asymptomatic School Children in Madrid, Spain, November 2017 to June 2018. Euro Surveill. 2019;24(43):1900241.
4. Sánchez A, Munoz M, Gómez N, et al. Molecular epidemiology of Giardia, Blastocystis and Cryptosporidium among indigenous children from the Colombian Amazon Basin. Front Microbiol. 2017;8:248.
5. Maryanti E, Lesmana SD, Mandela H. Deteksi Protozoa Usus Oportunistik pada Penderita Diare Anak di Puskesmas Rawat Inap Pekanbaru. Jurnal Ilmu Kedokteran. 2017;9(1):22–6.
6. Fauziah N, Aviani JK, Agrianfanny YN, et al. Intestinal Parasitic Infection and Nutritional Status in Children under Five Years Old: A Systematic Review. Trop Med Infect Dis. 2022;7(11):371.
7. Abou-Seri H, Abdalgaber M, Zahran F. Enteric parasitic infections: From environmental enteric dysfunction to gut microbiota and childhood malnutrition. Parasitologists United Journal. 2022;15(3):216–23.
8. Kotloff KL. The Burden and Etiology of Diarrheal Illness in Developing Countries. Pediatr Clin North Am. 2017;64(4):799–814.
9. Rojas-Velázquez L, Morán P, Serrano-Vázquez A, et al. The regulatory function of Blastocystis spp. on the immune inflammatory response in the gut microbiome. Front Cell Infect Microbiol. 2022;12:967724.
10. Bora I, Dutta V, Lyngdoh WV, et al. Study of intestinal parasites among the immunosuppressed patients attending a tertiary-care center in Northeast India. Int J Med Sci Pub Health. 2016;5(5):924–9.
11. Guerrant RL, DeBoer MD, Moore SR, et al. The impoverished gut—a triple burden of diarrhoea, stunting and chronic disease. Nat Rev Gastroenterol Hepatol. 2013; 10(4):220–9.
12. Vilcins D, Sly PD, Jagals P. Environmental risk factors associated with child stunting: a systematic review of the literature. Ann Glob Health. 2018;84(4):551-562.
13. Zavala GA, García OP, Camacho M, et al. Intestinal parasites: Associations with intestinal and systemic inflammation. Parasite Immunol. 2018;40(4): e12518.
14. Yoseph A, Beyene H. The high prevalence of intestinal parasitic infections is associated with stunting among children aged 6–59 months in Boricha Woreda, Southern Ethiopia: a cross-sectional study. BMC Public Health. 2020;20(1):1270.
15. Sardinha-Silva A, Alves-Ferreira EV, Grigg ME (2022). Intestinal immune responses to commensal and pathogenic protozoa. Front Immunol, 13:963723.
16. Mohammed J, Shiferaw A, Zeleke A, et al. Prevalence and Associated Risk Factors of Intestinal Parasites among Diarrheic Under-Five Children Attending Bahir Dar and Han Health Centers, Northwest Ethiopia: A Cross-Sectional Study. J Parasitol Res. 2022;2022: 7066529.
17. Badan Penelitian dan Pengembangan Kesehatan Kementerian Kesehatan Republik Indonesia. Riset Kesehatan Dasar 2018. Badan Penelitian dan Pengembangan Kesehatan Kementerian Kesehatan Republik Indonesia; 2018. https://repository.badankebijakan.kemkes.go.id/id/eprint/3514/1/Laporan%20Riskesdas%202018%20Nasional.pdf
18. Ayana M, Cools P, Mekonnen Z, et al. Comparison of four DNA extraction and three preservation protocols for the molecular detection and quantification of soil-transmitted helminths in stool. PLoS Negl Trop Dis. 2019;13(10):e0007778.
19. Mardani Kataki M, Tavalla M, Beiromvand M. Higher prevalence of Blastocystis hominis in healthy individuals than patients with gastrointestinal symptoms from Ahvaz, southwestern Iran. Comp Immunol Microbiol Infect Dis. 2019;65:160–4.
20. Costache C, Kalmár Z, Colosi HA, et al. First Multilocus Sequence Typing (MLST) of Giardia duodenalis Isolates from Humans in Romania. Parasit Vectors. 2020;13(1):387.
21. Hajissa K, Islam MA, Sanyang AM, et al. Prevalence of intestinal protozoan parasites among school children in Africa: A systematic review and meta-analysis. PLoS Negl Trop Dis. 2022;16(2):e0009971.
22. Debash H, Alemu M, Bisetegn H. The prevalence of intestinal parasites, undernutrition and their associated risk factors among school-age children in Sekota Town, Northeast Ethiopia: A community-based cross-sectional study. Health Sci Rep. 2023;6(3):e1137.
23. Gabain IL, Ramsteijn AS, Webster JP. Parasites and Childhood Stunting – A Mechanistic Interplay with Nutrition, Anemia, Gut Health, Microbiota, and Epigenetics. Trends Parasitol. 2023;39(3):167–80.
24. Deka S, Kalita D, Hazarika N. Prevalence and Risk Factors of Intestinal Parasitic Infection in Under-Five Children with Malnutrition: A Hospital Based Cross-Sectional Study. J Family Med Prim Care. 2022;11(6):2794- 2801.
25. Gutiérrez-Jiménez J, Luna-Cázares LM, Martínez-de la Cruz L, et al. Children from a Rural Region in the Chiapas Highlands, Mexico, Show an Increased Risk of Stunting and Intestinal Parasitoses when Compared with Urban Children. Bol Med Hosp Infant Mex. 2019;76(1):18–26.
26. Wahdini S, Putra VP, Sungkar S. The Prevalence of Intestinal Protozoan Infections among Children in Southwest Sumba Based on the Type of Water Sources. Infect Chemother. 2021;53(3):519-527.
27. Rozi MF, Darlan DM, Rahmawati R, et al. Intestinal Parasitic Infections and Eosinophilia: A Cross-sectional Study among Primary School-aged Children in Medan, Indonesia. International Journal of Human and Health Sciences. 2020;4(4):277–81.
28. Cociancic P, Torrusio SE, Garraza M, et al. Intestinal Parasites in Child and Youth Populations of Argentina: Environmental Factors Determining Geographic Distribution. Rev Argent Microbiol. 2021;53(3):225–32.
29. Gozalbo M, Pavón A, Toledo R, et al. Epidemiological Study of Intestinal Parasitism in the Child Population of Department of Managua (Nicaragua). IJCMC. 2021;14(5):1–10.
30. Arshad S, Khatoon N, Warind JA, et al. The Prevalence of Human Intestinal Protozoal and Helminthic Infection in Karachi. Int J Biol Biotech. 2019;16(2):319–23.
31. Hussein JN, Meerkhan AA. The Incidence of Intestinal Parasites among Children in Hivi Pediatric Hospital, Duhok, Iraq. Science Journal of University of Zakho. 2019;7(1):1–4.
32. Khariri, Agtini MD, Ariyanti E, et al. Parasitic Infestation in the Incidence of Diarrhea among Toddlers in Jakarta, Bogor, Banjarmasin and Makassar. Proceedings of the 4th International Symposium on Health Research (ISHR 2019). 2020;658–62.
33. Yentur Doni N, Yildiz Zeyrek F, Simsek Z, et al. Risk Factors and Relationship Between Intestinal Parasites and the Growth Retardation and Psychomotor Development Delays of Children in Şanlıurfa, Turkey. Turkiye Parazitol Derg. 2015;39(4):270–6.
34. Ignatius R, Gahutu JB, Klotz C, et al. High Prevalence of Giardia duodenalis Assemblage B Infection and Association with Underweight in Rwandan Children. PLoS Negl Trop Dis. 2012;6(6):e1677.
35. Shaima SN, Das SK, Ahmed S, et al. Anthropometric Indices of Giardia-Infected Under-Five Children Presenting with Moderate-to-Severe Diarrhea and Their Healthy Community Controls: Data from the Global Enteric Multicenter Study. Children (Basel). 2021; 8(12):1186.
36. Afridi MF, Farhat K, Ali S, et al. Prevalence of Intestinal Parasitic Infestations in Relation to Wasting among Children Under 5 Years of Age in Skardu, Pakistan: A Cross-Sectional Observational Study. Isra Med J. 2021;13(2):130–3.
37. Fakhri Y, Daraei H, Ghaffari HR, et al. The risk factors for intestinal Giardia spp infection: Global systematic review and meta-analysis and meta-regression. Acta Trop. 2021; 220:105968.
38. Zonta ML, Cociancic P, Oyhenart EE, et al. Intestinal Parasitosis, Undernutrition and Socio-Environmental Factors in Schoolchildren from Clorinda Formosa, Argentina. Rev Salud Publica (Bogota). 2019; 21(2):224–31.
39. Kantzanou M, Karalexi MA, Vrioni G, et al. Prevalence of intestinal parasitic infections among children in Europe over the last five years. Trop Med Infect Dis. 2021;6(3):160.
40. Ghani MKA, Alharizi T. Blastocystosis amongst the Orang Asli (Aborigine) Schoolchildren at Pos Senderut, Kuala Lipis, Malaysia. Int Med J. 2021;28(2):217–9.
41. Deng Y, Zhang S, Ning C, et al. Molecular Epidemiology and Risk Factors of Blastocystis sp. Infections among General Populations in Yunnan Province, Southwestern China. Risk Manag Healthc Policy. 2020;13:1791-1801.
42. Athiyyah AF, Surono IS, Ranuh RG, et al. Mono-Parasitic and Poly-Parasitic Intestinal Infections among Children Aged 36–45 Months in East Nusa Tenggara, Indonesia. Trop Med Infect Dis. 2023;8(1):45.
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| Issue | Vol 20 No 2 (2025) | |
| Section | Original Article(s) | |
| Keywords | ||
| Blastocystis hominis Children Giardia duodenalis Intestinal protozoan infection Stunting | ||
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How to Cite
1.
Fauziah N, Sari I, Faridah L, Afriandi I, Adrizain R, Nugraha N, Kurniawan A. Risk Factor of Blastocystis hominis and Giardia duodenalis among Stunted Children in Bandung Regency, Indonesia. Iran J Parasitol. 2025;20(2):289-298.
