Sains Malaysiana 51(12)(2022): 4185-4195

http://doi.org/10.17576/jsm-2022-5112-25

 

The Effect of Probiotic Biscuit on Faecal Microbiota in Malnourished Children

(Kesan Biskut Probiotik kepada Mikrobiota Najis dalam Kalangan Kanak-kanak Kurang Nutrisi)

 

ANNIS CATUR ADI1,*, CLARA KUSHARTO2 & SRI ANNA MARLIYATI2

 

1Department of Nutrition, Faculty of Public Health, Universitas Airlangga, 60115

Surabaya, East Java, Indonesia

2Faculty of Human Ecology, Bogor Agricultural University, 16680 Bogor, West Java, Indonesia

 

Received: 21 September 2021/Accepted: 23 September 2022

 

Abstract

A human intervention study on the effect of 90 days supplementation of creamed biscuit with the potential of containing probiotic strain E. faecium IS-27526 at a dose of 108cfu/day on Bifidobacterium in the faecal microbiota of malnourished children under 5 years was conducted. The study was a Randomized Double Blind Placebo Controlled Trial for children under five years old. There were 5 groups with 6 children each: P0 = control biscuit with control cream; P1 = fish and soy protein isolate biscuit with control cream; P2 = control biscuit with probiotic cream; P3 = fish and soy protein isolate biscuit with probiotic cream (every day) and P4 = fish and soy protein isolate biscuit with probiotic cream (every two days). PCR was used to detect Bifidobacterium and Enterococcus faecium in faeces samples.  It was concluded after 90 days of supplementation, only 25% of children in the controlled group (P0) harboured Bifidobacterium. In treated groups P1 and P4, the percentage of children positive for Bifidobacterium was approximately 60%, while in groups P2 and P3 the prevalence was 100%. However, the increase of 10% was only demonstrated by P3 as 100% of Bifidobacterium content has been shown in group P2 at the pre-treatment condition.  In the controlled group (P0), E. faecium could not be identified either pre or post-intervention, in contrast to the treated groups which showed an increase in some treatments with the highest of 66.7% (group P3). No adverse effect was observed during 90 days of supplementation to children. In conclusion, supplementation of fish and soy protein isolate biscuit and/or probiotic cream every day at a dose of 108cfu/day is considered safe for children under five years old and even increased the number of samples with the presence of bifidobacteria and E. faecium in the fecal microbiota.

 

Keywords: Bifidobacterium; Enterococcus faecium; malnourished; microbiota; probiotic cream

 

Abstrak

Kajian campur tangan manusia terhadap kesan suplemen 90 hari biskut berkrim dengan potensi mengandungi strain probiotik E. faecium IS-27526 pada dos 108cfu/hari pada Bifidobakteria dalam mikrobiota najis kanak-kanak kurang zat makanan di bawah 5 tahun telah dijalankan. Kajian ini ialah Percubaan Rawak Terkawal Dwibuta Plasebo untuk kanak-kanak di bawah umur lima tahun. Terdapat 5 kumpulan dengan 6 kanak-kanak setiap satu: P0 = biskut kawalan dengan krim kawalan; P1 = biskut pencilan protein ikan dan soya dengan krim kawalan; P2 = biskut kawalan dengan krim probiotik; P3 = biskut pencilan protein ikan dan soya dengan krim probiotik (setiap hari) dan P4 = biskut pencilan protein ikan dan soya dengan krim probiotik (setiap dua hari). PCR digunakan untuk mengesan Bifidobakteria dan Enterococcus faecium dalam sampel najis. Kesimpulannya, selepas 90 hari suplemen, hanya 25% kanak-kanak dalam kumpulan terkawal (P0) memendam Bifidobacterium. Dalam kumpulan rawatan P1 dan P4, peratusan kanak-kanak positif Bifidobakteria adalah kira-kira 60% manakala dalam kumpulan P2 dan P3 prevalens adalah 100%. Walau bagaimanapun, peningkatan sebanyak 10% hanya ditunjukkan oleh P3 kerana 100% kandungan Bifidobakteria telah ditunjukkan dalam kumpulan P2 pada keadaan pra-rawatan. Dalam kumpulan kawalan (P0), E. faecium tidak dapat dikenal pasti sama ada sebelum atau selepas intervensi, berbeza dengan kumpulan yang dirawat yang menunjukkan peningkatan dalam beberapa rawatan dengan tertinggi sebanyak 66.7% (kumpulan P3). Tiada kesan sampingan diperhatikan semasa 90 hari pemberian suplemen kepada kanak-kanak. Kesimpulannya, penambahan biskut pencilan protein ikan dan soya dan/atau krim probiotik setiap hari pada dos 108cfu/hari dianggap selamat untuk kanak-kanak di bawah umur lima tahun malah menambah bilangan sampel dengan kehadiran bifidobakteria dan E. faecium dalam mikrobiota najis.

 

Kata kunci: Bifidobakteria; Enterococcus faecium; krim probiotik; kurang zat; mikrobiota

 

REFERENCES

Adeyeye, S.A.O., Adebayo-Oyetoro, A.O. & Omoniyi, S.A. 2017. Quality and sensory properties of maize flour cookies enriched with soy protein isolate. Cogent Food & Agriculture 3: 1278827.

Adi, A.C. 2010. Efficacy of biscuit enriched with the catfish protein flour (Clarias gariepinus), soy protein isolate and Enterococcus faecium IS-27526 microencapsulated probiotic as a supplementary food on underweight under-five children (2-5 years old). Dissertation. Postgraduate, Bogor Agricutural University, Bogor (Unpublished).

Agustina, R., Bovee-Oudenhoven, I.M.J., Lukito, W., Fahmida, U., van de Rest, O., Zimmermann, M.B., Firmansyah, A., Wulanti, R., Albers, R., van den Heuvel, E.G.H.M. & Kok, F.J. 2013. Probiotics Lactobacillus reuteri DSM 17938 and Lactobacillus casei CRL 431 modestly increase growth, but not iron and zinc status, among Indonesian children aged 1-6 years. The Journal of Nutrition 143(7): 1184-1193. https://doi.org/10.3945/jn.112.166397

Arnold, M., Rajagukguk, Y.V. & Gramza-Michalowska, A. 2021. Characterization of Dadih: Traditional fermented buffalo milk of Minangkabau. Beverages 7(3): 60. https://doi.org/10.3390/beverages7030060

Cano, P.G., Aguero, G. & Perdigon, G. 2002. Immunological effect of yogurt addition to re-nutritrion diet in a malnutrition experimental model. Journal of Dairy Research 69: 303-316.

Cencic, A. & Chingwaru, W. 2010. The role of functional foods, nutraceuticals, and food supplements in intestinal health. Nutrients 2: 611-625. doi: 10.3390/nu2060611

Chung, H-J., Nguyen, T.T.B., Kim, H-J. & Hong, S-T. 2018. Gut microbiota as a missing link between nutrients and traits of human. Front. Microbiol. 9: 1510. doi: 10.3389/fmicb.2018.01510

Dargahi, N., Johnson, J., Donkor, O., Vasiljevic, T. & Apostolopoulos, V. 2019.  Immunomodulatory effects of probiotics: Can they be used to treat allergies and autoimmune diseases? Maturitas 119: 25-38. 

Diah Ikasari, Ema Hastarini & Theresia Dwi Suryaningrum. 2020. Characteristics of cookies formulated with fish protein concentrate powder produced from snakehead fish (Channa striata) extraction by product. E3S Web of Conferences. p. 147.

Dieterich, W., Schink, M. & Zopf, Y. 2018. Microbiota in the gastrointestinal tract. Medical Science 6(4): 116.

Dudley, D.J. 2020. The placental microbiome: Yea, nay or maybe? Brit. J. Obstet. Gynecol. 127: 170.

EFSA Panel on Additive and Products or Substances used in Animal Feed (FEEDAP), Rychen, G., Aquilina, G., Azimonti, G., Bampidis, V., de Lourdes Bastos, M., Bories, G., Chesson, A. Cocconcelli, P.S., Flachowsky, G., Gropp, J., Kolar, B., Kouba, M., López-Alonso, R., López Puente, S., Mantovani, A., Mayo, B., Ramos, F., Saarela, M., Villa, R.E., Wallace, R.J., Wester, P., Glandort, B., Herman, L., Kärenlampi, S., Aguilera, J., Anguita, M., Brozzi, R. & Galobart, J. 2018. Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA J16(3): e05206.

Freitas, A.C. & Hill, J.E. 2018. Bifidobacteria isolated from vaginal and gut microbiomes are indistinguishable by comparative genomics. PLoS ONE 13: e0196290.

Harianti, R. 2009.  Effect of hight protein biscuit with probiotic cream to microbiota fecal profile and weight rat. Thesis. Postgraduate, Bogor Agricultural University, Bogor (Unpublished).

Harnavi, H., Yan, W., Bambang, P. & Endang, P. 2020. Characterization of lactic acid bacteria and determination of antimicrobial activity in dadih from air dingin alahan Panjang District, Solok Regency-West Sumatera. Systematic Reviews in Pharmacy 11(3): 583-586.

Harnentis, Nurmiati, Yetti Marlida, Frederick Adzitey & Nurul Huda 2019. γ-Aminobutyric acid production by selected lactic acid bacteria isolate of an Indonesian indigenous fermented buffalo milk (dadih) origin. Veterinary World 12(8): 1352-1357.

Horison, R. & Surono, I.S. 2020. Half-life estimation of encapsulated Enterococcus faecium IS-27526 by Accelerated Shelf Life Testing (ASLT). IOP Conference Series: Earth and Environmental Science. p. 426.

Indonesia Ministry of Health. 2018. Basic Health Survey Report (RISKESDAS) Indonesia.

Indonesia Ministry of Health. 2013. Basic Health Survey Report (RISKESDAS) Indonesia.

Jeong, D., Kim, D.H., Kang, I.B., Kim, H., Song, K.Y., Kim, H.S. & Seo, K.H. 2017. Modulation of gut microbiota and increase in fecal water content in mice induced by administration of Lactobacillus kefiranofaciens DN1. Food Funct. 8: 680-686.

Khan, A., Khan, S., Jan, A.A. & Khan, M. 2017. Health complication caused by protein deficiency. Journal of Food Science Nutrition 1(1): 1-2.

Kim, D.H., Chon, J.W., Kim, H. & Seo, K.H. 2015. Modulation of intestinal microbiota in mice by kefir administration. Food Sci. Biotechnol. 24: 1397-1403.

Kim, D.H., Jeong, D., Kang, I.B., Kim, H., Song, K.Y. & Seo, K.H. 2017. Dual function of Lactobacillus kefiri DH5 in preventing high-fat-diet-induced obesity: Direct reduction of cholesterol and upregulation of PPAR-a in adipose tissue. Mol. Nutr. Food Res. 61: 1700252.

Kim, D.H., Kim, H., Jeong, D., Kang, I.B., Chon, J.W., Kim, H.S., Song, K.Y. & Seo, K.H. 2017. Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: Targeted and untargeted community analysis with correlation of biomarkers. J. Nutr. Biochem. 44: 35-43.

Kusharto, C.M., Astawan, M., Marliyati, S.A. & Amalia, L. 2009. Functional food base on fish protein and probiotic for increasing immunity on nutrition vulnerable under five children. Research Report. Bogor: Bogor Agricultural University.

Lin, C., Lin, Y., Zhang, H., Wang, G., Zhao, J., Zhang, H. & Chen, W. 2022. Intestinal ‘infant-type’ bifidobacteria mediate immune system development in the first 1000 days of life. Nutrients 14(7): 1498.

Lu, L. & Walker, W.A. 2001. Phatologic and phisiologic interaction of bacteria with the gastrointestinal ephitelium. Am. J. Clin. Nutr. 73(suppl): 1124S-1130S.

Lwanga, S.K. & Lemeshow, S. 1991. Sample Size Determination in Health Studies: A Practical Manual. Geneva: World Health Organization.

Mahooti, M., Abdolalipour, E., Salehzadeh, A., Mohebbi, S.R., Gorji, A. & Ghaemi, A. 2019. Immunomodulatory and prophylactic effects of Bifidobacterium bifidum probiotic strain on influenza infection in mice. World J. Microbiol. Biotechnol35: 1-9. 

Maldonado, G.C., Cazorla, S.I., Lemme, D.J.M., Velez, E. & Perdigon, G. 2019. Beneficial effects of probiotic consumption on the immune system. Ann. Nutr. Metab. 74: 115-124.

Matsuki, T., Watanabe, K., Fujimoto, J., Kado, Y., Takada, T., Matsumoto, K. & Tanaka, R. 2004. Quantitative PCR with 16S rRNA-gene-targeted species-specific primers for analysis of human intestinal Bifidobacteria. Applied and Enviromental Microbiology 20(1): 167-173.

Nkamga, V.D., Henrissat, B. & Drancourt, M. 2017. Archaea: Essential inhabitants of the human digestive microbiota. Human Microbiome Journal 3: 1-8.

Onubi, O.J., Poobalan, A.S., Dineen, B., Marais, D. & McNeill, G. 2015. Effects of probiotics on child growth: A systematic review. Journal of Health, Population and Nutrition 34(8).

Piirainen, L., Kekkonen, R.A., Kajander, K., Ahlroos, T., Tynkkynen, S., Nevala, R. & Korpela, R. 2008. In school-aged children a combination of galacto-oligosaccharides and Lactobacillus GG increases bifidobacteria more than Lactobacillus GG on its own.  Annals of Nutrition & Metabolisme 52(3): 204-208.

Rana, J., Uddin, J., Peltier, R. & Oulhote, Y. 2019. Associations between indoor air pollution and acute respiratory infections among under-five children in Afghanistan: Do SES and Sex Matter? Int. J. Environ. Res. Public Health 16(16): 2910. https://doi.org/10.3390/ijerph16162910

Regulation of Indonesian Minister of Health Number 2 of 2020 concerning Child Anthropometry Standards. Jakarta. 2020.

Rinninella, E., Raoul, P., Cintoni, M., Franceschi, F., Miggiano, G.A.D., Gasbarrini, A. & Mele, M.C. 2019. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and disease. Microorganisms 7(1): 14.

Robertson, R.C., Manges, A.R., Finlay, B.B. & Prendergast, A.J. 2019. The human microbiome and child growth - First 1000 days and beyond. Trends Microbiol. 27: 131-147. doi: 10.1016/j.tim.2018.09.008

Roza, E., Aritonang, S.N., Yellita, Y., Susanty, H., Rizqan & Pratama, Y.E. 2022. Potential of dadiah kapau from Agam District, West Sumatra, Indonesia as a source of probiotics for health. Biodiversitas 23(1): 564-571.

Siegrist, M. & Hartmann, C. 2020. Consumer acceptance of novel food technologies. Nature Food 1: 343-350.

Siti Helmyati, Karina Muthia Shanti, Fahmi Tiara Sari, Martha Puspita Sari, Dominikus Raditya Atmaka, Rio Aditya Pratama, Maria Wigati, Setyo Utami Wisnusanti, Fatma Zuhrotun Nisa’ & Endang Sutriswati Rahayu. 2021. Synbiotic fermented milk with double fortification (Fe-Zn) as a strategy to address stunting: A randomized controlled trial among children under five in Yogyakarta, Indonesia. Processes 9(3): 543. https://doi.org/10.3390/pr9030543

Skalkam, M.L., Wiese, M., Nielsen, D.S. & van Zanten, G. 2016. Chapter 33 - In vitro screening and evaluation of synbiotics. In Probiotics, Prebiotics, and Synbiotics, edited by Watson, R.R. & Preedy, V.R.  Massachusetts: Academic Press. pp. 477-486.

Sukabumi Department of Health. 2012. Health Profile of Sukabumi.

Surono, I.S. 2016. Probiotic, Microbiome and Functional Food. Deepublish: Yogyakarta.

Umu, Ö.C.O., Rudi, K. & Diep, D.B. 2017. Modulation of the gut microbiota by prebiotic fibres and bacteriocins. Microb. Ecol. Health Dis. 28: 1348886. doi: 10.1080/16512235.2017.1348886

Wang, Y., Qin, S., Jia, J., Huang, L., Li, F., Jin, F., Ren, Z. & Wang, Y. 2019. Intestinal microbiota-associated metabolites: Crucial factors in the effectiveness of herbal medicines and diet therapies. Front. Physiol. 10: 1343. doi: 10.3389/fphys.2019.01343

Wirawati, C.U., Sudarwanto, M.B., Lukman, D.W. & Wientarsih, I. 2017. Characteristic and development of cow’s milk dadih as an alternate of buffalo’s milk dadih. WARTAZOA 27(2): 95-103.

Zucko, J., Starcevic, A., Diminic, J., Oros, D., Mortazavian, A.M. & Putnik, P. 2020. Probiotic-friend or foe? Current Opinion in Food Science 32: 45-49.

 

*Corresponding author; email: annis_catur@fkm.unair.ac.id

 

 

 

 

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