Profiling of the intestinal microbiota of stunted children in Semarang, Indonesia
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
##plugins.themes.bootstrap3.article.main##
Abstract
Abstract. Susanti R, Zaenafreee I, Christijanti W, Mustikaningtyas D, Yuniastuti A. 2024. Profiling of the intestinal microbiota of stunted children in Semarang, Indonesia. Biodiversitas 25: 1337-1343. Stunting is a top global health priority. Gut microbiota profiles correlate with growth biomarkers, including stunting. This study aims to profile the intestinal microbiota of stunted children in Semarang, Indonesia. This research is an observational analytical study with a cross-sectional design, conducted on children aged 3-3.5 years with stunting and normal nutritional status in Bandarharjo Village, North Semarang District, Semarang City, Central Java Province, Indonesia. Fecal samples were collected, kept in a cooler box, and taken to the laboratory to be analyzed for pH, worm eggs, Alpha-1-Antitrypsin (AAT) levels, and microbiota profile. Microbial DNA was extracted from stool samples. The diversity and abundance of the gut microbiota were determined using the 16S rRNA V3-V4 gene marker region. The diversity and abundance of the intestinal microbiota of stunted children are smaller than those of non-stunted children. The ratio of Firmicutes/Bacteroidetes in intestinal stunting is 96.45, while in healthy, it is 26.05. The intestinal microbes of healthy children were dominated by Lactobacillus rhamnosus (30.92%) and Bifidobacterium breve (21.49%). The intestinal microbiota of stunted children is dominated by the bacterial species Blautia obeum (23.5%) and Faecalibacterium prausnitzii (19.13%). The concentration of AAT in the feces of stunted children is higher (75.49±7.68) than that of healthy children (26.73±4.48). The pH value of the feces of stunted children was higher (6.84±0.31) than that of healthy children (6.29±0.43). In conclusion, the composition of the microbiota indicates a condition of dysbiosis in intestinally stunted children. The intestines of stunted children may experience inflammation based on data on higher pH values, higher AAT levels, and deficiencies in bacterial species that benefit the host.
##plugins.themes.bootstrap3.article.details##
References
Arini D, Nursalam N, Mahmudah M, Faradilah I. 2020. The incidence of stunting, the frequency/duration of diarrhea and Acute respiratory infection in toddlers. J Public health Res 9(2): 117-120. DOI: 10.4081/jphr.2020.1816
Benvenuto AF, Adnyana IGA, Samodra VM, Azmi F. 2022. The relationship between worm infection and stunting in children in Central Lombok Regency, West Nusa Tenggara Province. Jurnal Aisyah, Jurnal Ilmu Kesehatan 7(2): 663-668. DOI: 10.30604/jika. v7i2.1483
Black RE, Victora CG, Walker SP, Bhutta ZA, Christian P, de Onis M, Ezzati M, Grantham-McGregor S, Katz J, Martorell R, Uauy R, Maternal and Child Nutrition Study Group. 2013. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 382(9890): 427-451. DOI: 10.1016/S0140-6736(13)60937-X
Bourdon C, Lelijveld N, Thompson D, Dalvi PS, Gonzales GB, Wang D, Alipour M, Wine E, Chimwezi E, Wells JC, Kerac M, Bandsma R, Nyirenda M.J. 2019. Metabolomics in plasma of Malawian children 7 years after surviving severe acute malnutrition: “ChroSAM” a cohort study. EBioMedicine 45: 464-472. DOI: 10.1016/j.ebiom. 2019.06.041
Callahan BJ, Mcmurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holman SP. 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13 (7): 581-583. DOI: 10.1038/nmeth.3869.
Canfora EE, van der Beek CM, Jocken JWE, Goossens GH, Holst JJ, Damink SWM, Lenaerts K, Dejong CHC, Blaak EE. 2017. Colonic infusions of short-chain fatty acid mixtures promote energy metabolism in overweight/obese men: a randomized crossover trial. Sci Rep 7(1): 2360. DOI: 10.1038/s41598- 017-02546-x.
Canfora EE, Meex RCR, Venema K, Blaak EE. 2019. Gut microbial metabolites in obesity, NAFLD and T2DM. Nat Rev Endocrinol 15(5): 261-273. DOI: 10.1038/s41574- 019-0156-z.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (5): 335-336. DOI: 10.1038/nmeth.f.303.
Central Bureau of Statistics-Ministry of Health Indonesia. 2019. Report on integration of economic social survey (susenas) implementation, March 2019 and nutritional status of children younger than five study in Indonesia (SSGBI). Jakarta. (in Indonesian).
Cionci NB, Baffoni L, Gaggìa F, Di Gioia D. 2018. Therapeutic microbiology: the role of Bifidobacterium breve as food supplement for the prevention/treatment of paediatric diseases. Nutrients 10(11): 1723. DOI: 10.3390/nu10111723
Collender PA, Kirby AE, Addiss DG, Freeman MC, Remais JV. 2015. Methods for quantification of soil-transmitted helminths in environmental media: current techniques and recent advances. Trends Parasitol 31(12): 625-639. DOI: 10.1016/j.pt.2015.08.007
de Onis M, Branca F. 2016. Childhood stunting: a global perspective. Matern Child Nutr 12 (Suppl 1): 12-26. DOI: 10.1111/mcn.12231
Ezeh OK, Abir T, Zainol NR, Mamun A Al, Milton AH, Haque MR, Agho KE. 2021. Trends of stunting prevalence and its associated factors among Nigerian children aged 0-59 months residing in the northern Nigeria, 2008-2018. Nutrients 13(12):3412. DOI: 10.3390/nu13124312
Gehrig JL, Venkatesh S, Chang HW, Hibberd MC, Kung VL, Cheng J, Chen RY, Subramanian S, Cowardin CA, Meier MF, O'Donnell D, Talcott M, Spears LD, Semenkovich CF, Henrissat B, Giannone RJ, Hettich RL, Ilkayeva O, Muehlbauer M, Newgard CB, … Gordon JI. 2019. Effects of microbiota directed foods in gnotobiotic animals and undernourished children. Science 365(6449): eaau4732. DOI: 10.1126/science.aau4732
Guida S, Venema K. 2015. Gut microbiota and obesity: involvement of the adipose tissue. J Funct Foods 14: 407-423.
Hoffman DJ, Campos-Ponce M, Taddei CR, Doak CM. 2017. Microbiome, growth retardation and metabolism: are they related? Ann Hum Biol 44(3): 201-207. DOI: 10.1080/ 03014460.2016.1267261
Holm JB, Humphrys MS, Robinson CK, Settles ML, Ott S, Fu L, Yang H, Gajer P, He X, McComb E, Gravitt PE, Ghanem KG, Brotman RM, Ravel J. 2019. Ultrahigh-throughput multiplexing and sequencing of >500 basepair amplicon regions on the illumina HiSeq 2500 platform. mSystems 4(1): e00029. DOI:10.1128/msystems. 0002919
Hossain MS, Das S, Gazi MA, Alam MA, Haque NMS, Mahfuz M, Ahmed T, Damman CJ. 2019. Association of faecal pH with childhood stunting: results from a cross-sectional study. BMJ Paediatr Open 3(1): e000549. DOI:10.1136/bmjpo-2019-000549
Hunter JD. 2007. Matplotlib: A 2D graphics environment. Comput Sci Eng. 9(3): 99-104. DOI: 10.1109/MCSE.2007.55
Indonesian Ministry of Health. 2023. Stunting prevalence in Indonesia decreases to 21.6% from 24.4% (In Indonesian). https://sehatnegeriku.kemkes.go.id/baca/rilis-media/20230125/ 3142280/prevalensi-stunting-di-indonesia-turun-ke-216-dari-244/.
Indonesian Ministry of Health. 2020. Indonesia health profile 2019. https://pusdatin.kemkes. go.id/resources/download/pusdatin/profil-kesehatan-indonesia/Profil-Kesehatan- Indonesia-2019. pdf. Accessed 10 Sep 2021.
Kolde R, Franzosa EA, Rahnavard G, Hall AB, Vlamakis H, Stevens C, Daly MJ, Xavier RJ, Huttenhower C. 2018. Host genetic variation and its microbiome interactions within the human microbiome project. Genome Med. 10(1): 6. DOI: 10.1186/s13073-018-0515-8
Kulakov D, Knyazev O, Lishchinskaya A, Kagramanova A, Noscova K, Zvyaglova M, Shkurko T, Nanaeva B. 2022. Alpha-1 antitrypsin is a marker of increased intestinal permeability in ulcerative colitis and COVID-19 infection. Am J Gastroenterol 117(1): S9-S9. DOI: 10.14309/01.ajg.0000897640.00775.30
Kumar M, Ji B, Babaei P, Das P, Lappa D, Ramakrishnan G, Fox TE, Haque R, Petri WA, Bäckhed F, Nielsen J. 2018. Gut microbiota dysbiosis is associated with malnutrition and reduced plasma amino acid levels: Lessons from genome-scale metabolic modeling. Metab Eng. 49: 128-42. DOI: 10.1016/j.ymben.2018.07. 018
Lopez-Siles M, Duncan S, Garcia-Gil L, Martinez-Medina M. 2017. Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J 11: 841-852. DOI: 10.1038/ismej.2016.176
Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R. 2020. The Firmicutes/Bacteroidetes ratio: A relevant marker of gut dysbiosis in obese patients?. Nutrients 12 (5): 1474. DOI: 10.3390/nu12051474.
Masrul M, Izwardy D, Sudji IR, Purnakarya I, Syahrial S, Nindrea RD. 2020. Microbiota profile with stunting children in West Sumatera Province, Indonesia. Maced J Med Sci 8(E):334-340. DOI: 10.3889/oamjms.2020.4209
Mathipa-Mdakane MG, Thantsha MS. 2022. Lacticaseibacillus rhamnosus: a suitable candidate for the construction of novel bioengineered probiotic strains for targeted pathogen control. Foods (Basel, Switzerland) 11(6): 785. DOI:10.3390/foods11060785
Mbuya MNN, Humphrey JH. 2016. Preventing environmental enteric dysfunction through improved water, sanitation and hygiene: an opportunity for stunting reduction in developing countries. Matern Child Nutr. 12:106-120. DOI: 10.1111/mcn.12220
McDonald D, Price MN, Goodrich J, Nawrocki EP, Desantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610-618. DOI: 10.1038/ismej.2011.139
Mendez-Salazar EO, Ortiz-Lopez MG, Granados-Silvestre MDLA, Palacios-Gonzalez B, Menjivar M. 2018. Altered gut microbiota and compositional changes in Firmicutes and Proteobacteria in Mexican undernourished and obese children. Front Microbiol. 9:1-11. DOI: 10.3389/fmicb.2018.02494
Nasrin D, Liang Y, Powell H, Casanova IG, Sow SO, Hossain MJ, Omore R, Sanogo D, Tamboura B, Zaman SMA, Antonio M, Jones JCM, Awuor AO, Kasumba IN, Ochieng JB, Badji H, Verani JR, Widdowson MA, Roose A, Jamka LP, Tennant SM, Ramakrishnan U, Kotloff KL. 2023. Moderate-to-severe diarrhea and stunting among children younger than 5 years: findings from the vaccine impact on diarrhea in Africa (VIDA) study. Clin Infect Dis 76: S41-S48. DOI: 10.1093/cid/ciac945
Pham TPT, Raoult D, Million M. 2019. IGF1 levels in children with severe acute malnutrition after nutritional recovery: a good predictor for children’s long-term health status. EbioMedicine 45:9-10. DOI: 10.1016/j.ebiom.2019.07.011.
Ramakrishna BS. 2013. Role of the gut microbiota in human nutrition and metabolism. J Gastroenterol Hepatol 4: 9-17. DOI: 10.1111/jgh.12294
Rinanda T, Riani C, Artarini A, Sasongko L. 2023. Correlation between gut microbiota composition, enteric infections and linear growth impairment: a case–control study in childhood stunting in Pidie, Aceh, Indonesia. Gut Pathogens 15:54 (1-14). DOI: 10.1186/s13099-023-00581-w
Rodrigues VF, Elias-Oliveira J, Pereira ÍS, Pereira JA, Barbosa SC, Machado MSG, Carlos D. 2022. Akkermansia muciniphila and gut immune system: a good friendship that attenuates inflammatory bowel disease, obesity, and diabetes. Front Immunol 13: 934695. DOI: 10.3389/fimmu.2022.934695
Sakamoto S, Putalun W, Vimolmangkang S, Phoolcharoen W, Shoyama Y, Tanaka H, Morimoto S. 2018. Enzyme-linked immunosorbent assay for the quantitative/qualitative analysis of plant secondary metabolites. J Nat Med 72(1): 32-42. DOI: 10.1007/s11418-017-1144-z
Schofield WB, Palm NW. 2018. Gut microbiota: IgA protects the pioneers. Curr Biol 28 (18): R1117-R1119. DOI: 10.1016/j.cub.2018.08.019.
Setyani LI, Anwar K. 2022. The association between feeding practices and history of diarrhea with nutritional status of toddlers. Indones J Public Heal Nutr 3:43-49. DOI: 10.7454/ijphn.v3i1.6171
Surono IS, Widiyanti D, Kusumo PD, Venema K. 2021. Gut microbiota profile of Indonesian stunted children and children with normal nutritional status. PLoS ONE. 16: 1-18. DOI: 10.1371/journal.pone.0245399
Turroni F, Duranti S, Milani C, Lugli GA, van Sinderen D, Ventura M. 2019. Bifidobacterium bifidum: a key member of the early human gut microbiota. Microorganisms 7(11): 544. DOI: 10.3390/microorganisms7110544
Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. 2020. The controversial role of human gut Lachnospiraceae. Microorganisms 8(4):1-25. DOI: 10.3390/microorganisms8040573
Vonaesch P, Randremanana R, Gody JC, Collard JM, Giles-Vernick T, Doria M, Vigan-Womas I, Rubbo PA, Etienne A, Andriatahirintsoa EJ, Kapel N, Brown E, Huus KE, Duffy D, Finlay BB, Hasan M, Hunald FA, Robinson A, Manirakiza A, Wegener-Parfrey L, Vray M, Sansonett PJ. 2018a. Identifying the etiology and pathophysiology underlying stunting and environmental enteropathy: study protocol of the Afribiota project. BMC Pediatr 18(1): 236 (1-18). DOI: 10.1186/s12887- 018-1189-5.
Vonaesch P, Morien E, Andrianonimiadana L, Sanke H, Mbecko JR, Huus KE, Naharimanananirina T, Gondje BP, Nigatoloum SN, Vondo SS, Kandou JEK, Randremanana R, Rakotondrainipiana M, Mazel F, Djorie SG, Gody JC, Finlay BB, Rubbo PA, Parfrey LW, Collard JM, Afribiota Investigators. 2018b. Stunted childhood growth is associated with decompartmentalization of the gastrointestinal tract and overgrowth of oropharyngeal taxa. Proc Natl Acad Sci USA 115(36): E8489-E98. DOI: 10.1073/pnas.1806573115
Wasihun AG, Dejene TA, Teferi M, Marugán J, Negash L, Yemane D, McGuigan KG. 2018. Risk factors for diarrhoea and malnutrition among children under the age of 5 years in the Tigray Region of Northern Ethiopia. PLoS ONE 13(11):32-39. DOI: 10.1371/journal.pone.0207743
World Health Organization. 2009. WHO child growth standards and the identification of severe acute malnutrition in infants and children—A Joint Statement by the World Health Organization and the United Nations Children’s Fund. available at: https://www.who.int/nutrition/publications/severemalnutrition/ 9789241598163/en/
World Health Organization. 2018. Global targets to improve maternal, infant and young child nutrition for 2025. Available at https://www.who.int/nutrition/topics/nutrition _globaltargets2025/en/
World Health Organization. 2021. Levels and trends in child malnutrition: UNICEF/WHO/The World Bank Group joint child malnutrition estimates: key findings of the 2021 edition. https://www.who.int/publications/i/item/9789240025257.
World Health Organization. 2023. Soil-transmitted helminth infections. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections. Accessed 19 February 2024.
Yadav M, Verma MK, Chauhan NS. 2018. A review of metabolic potential of human gut microbiome in human nutrition. Arch Microbiol 200: 203-217. DOI: 10.1007/s00203-017-1459-x
Yao S, Zhao Z, Wang W, Liu X. 2021. Bifidobacterium longum: protection against inflammatory bowel disease. J Immunol Res 2021: 8030297. DOI: 10.1155/2021/ 8030297
Most read articles by the same author(s)
- R. SUSANTI, AGUSTIN DIAN KARTIKASARI, FITRI ARUM SASI, DYKEN DWI ARLINDA, Genetic diversity of Central Javanese duck (Indonesia) based on Inter Simple Sequence Repeat markers , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 4 (2022)
- R. SUSANTI, RETNO SRI ISWARI, FIDIA FIBRIANA, INDRIAWATI INDRIAWATI, The duck cytochrome oxidase I (COI) gene: Sequence and patterns analysis for potential barcoding tool , Biodiversitas Journal of Biological Diversity: Vol. 19 No. 3 (2018)
- R. SUSANTI, WULAN CHRISTIJANTI, Effects of production system on the gut microbiota diversity and IgA distribution of Kampong chickens, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 2 (2022)
- R. SUSANTI, NAINA RIZKI KENARNI, ADI FRANATA JAYA, FARAH FITROTUN NISA’, RISKA LAILA MUKAROMAH, TALITHA WIDIATNINGRUM, NANA KARIADA TRI MARTUTI, MARGARETA RAHAYUNINGSIH, Microbial diversity in pesticidal and non-pesticidal paddy soil microbiomes , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 9 (2023)
- NOOR AINI HABIBAH, ARI YUNIASTUTI, R. SUSANTI, LISDIANA, DEWI MUSTIKANINGTYAS, ANANDA LUTFIAH, SISKA NA'ILIL AULIA, TAQQIYA RABBANI, Growth and production of secondary metabolites in the callus of Bima Brebes shallot varieties , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 8 (2024)
- R. SUSANTI, Polymorphic sequence in the ND3 region of Java endemic Ploceidae birds mitochondrial DNA , Biodiversitas Journal of Biological Diversity: Vol. 12 No. 2 (2011)
- R. SUSANTI, NUR RAHAYU UTAMI, ARI YUNIASTUTI , Characterization of microbiota and secretory Ig-A in the domestic duck (Anas platyrhynchos) small and large intestine , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 4 (2023)